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    Outdoor malaria vector species profile in dryland ecosystems of Kenya

    Study sites, sample collection and preparationAdult female mosquitoes used in this study had previously been collected from three areas: Kerio Valley (Baringo county), Rabai (Kilifi county) and Nguruman (Kajiado county) (Fig. 1), as part of vector-borne disease surveillance project and stored at – 80 °C at the International Centre of Insect Physiology and Ecology (icipe). The mosquitoes were surveyed between August 2019 and May 2020. Nguruman is an agropastoral area located in Kajiado county at the southern end of the Kenyan Rift Valley bordering Tanzania. The area has a semi-arid climate characterized by erratic rains, extreme temperatures, and cyclic and prolonged droughts30. The vegetation is dominated by bushland, grassland and open woodlands along seasonal river valleys. Specific indicator data for malaria is not available for Nguruman except for estimates pertaining to the larger Kajiado county which as of 2019 indicates a malaria incidence rate of 5 per 1000 population31. Collections in Kerio Valley (Baringo county within the Rift Valley) were conducted in Kapluk and Barwesa, both agro-pastoral areas with arid and semi-arid ecology. Malaria is a major vector-borne disease in the areas with report of perennially occurrence in neighboring riverine areas32. Rabai is one of the seven administrative sub-counties of Kilifi county in the coastal region of Kenya where malaria is endemic. The main economic activities in the area include subsistence agriculture, casual labor, crafts and petty trading. The weather patterns at the sites during the sampling period were as follows: Kerio Valley (mean daily temperature: 21.2 °C, mean daily rainfall: 4.1 mm, mean relative humidity: 73.4%); Rabai (mean daily temperature: 26.4 °C, mean daily rainfall: 2.1 mm; mean relative humidity: 78.1%) and Nguruman (mean daily temperature: 22.5 °C, mean daily rainfall: 0.9 mm, mean relative humidity: 61.2%).Mosquito survey and processingHost seeking mosquitoes were trapped using CDC light traps baited with dry ice (carbon dioxide) attractive to several mosquitoes. Traps were set outdoors about 10–15 m away from randomly selected homesteads from 18:00 h to 06:00 h. After collection, the mosquitoes were anesthetized with trimethylamine and temporarily stored in liquid nitrogen before transportation to the Emerging Infectious Disease (EID) laboratory at icipe and later stored at − 80 °C. Anopheline mosquitoes were morphologically identified to species level using published taxonomic keys15,33.DNA extraction and Anopheles species discriminationDNA was extracted from the head/thorax of individual mosquitoes using ISOLATE II Genomic DNA Extraction kit (Bioline, UK) following the manufacturer’s instructions and used for species discrimination and screening for P. falciparum infection and Gste2 mutations (described below).Cryptic sibling species of the Anopheles funestus and Anopheles gambiae complexes were identified using conventional PCR34,35 and/or sequencing. PCR for An. funestus complex in a 15 µl reaction volume comprised 0.5 µM of each primer targeting: Anopheles funestus s.s, Anopheles vaneedeni, Anopheles rivulorum, Anopheles parensis, Anopheles leesoni, Anopheles longipalpis A and Anopheles longipalpis C, 3 µl of 5X HOT FIREPol Blend Master Mix Ready to Load (Solis BioDyne, Estonia) and 2 µl of DNA template. The cycling conditions were initial denaturation at 95 °C for 15 min, and then 30 cycles of denaturation at 95 °C for 30 s, annealing at 46 °C for 30 s and extension at 72 °C for 40 s and final extension at 72 °C for 10 min. Size fragments of each species were scored after separation in 1.5% agarose gel electrophoresis stained with ethidium bromide against a 1 Kb DNA ladder (HyperLadder, Bioline, London, UK).For An. gambiae s.l., PCR in a 10 µl volume consisted of 2 µl of 5X Evagreen HRM Master Mix (Solis BioDyne, Estonia), 1 µl of DNA template and 10 µM concentration of each primer targeting An. gambiae s.s and An. arabiensis. The thermal cycling conditions included initial denaturation for 15 min at 95 °C followed by 40 cycles of denaturation at 95 °C for 20 s, annealing at 61 °C for 15 s and extension at 72 °C for 20 s followed by final extension at 72 °C for 7 min.A subset of An. funestus s.l. samples that failed to amplify using the established protocol, was further amplified and sequenced targeting the internal transcribed spacer 2 (ITS2) region of the ribosomal DNA (rDNA)36. This target has shown utility in discriminating closely related mosquito species including anophelines12 and sequences from diverse species for this marker are well represented in reference databases (e.g. GenBank). PCR volumes for rDNA ITS2 were 15 µl containing 0.5 µM of the forward and reverse primers, 3 µl of 5X HOT FIREPol Blend Master Mix Ready to Load (Solis BioDyne, Estonia) and 2 µl of DNA template. The cycling conditions were initial denaturation at 95 °C for 15 min, followed by 40 cycles of denaturation at 95 °C for 30 s, annealing at 60 °C for 30 s and extension at 72 °C for 45 s and final extension at 72 °C for 7 min. ExoSAP IT rapid cleanup kit (Affymetrix Inc., Santa Clara, CA, USA) was used to clean the PCR product as per the manufacturer’s guideline, and then outsourced for bidirectional Sanger sequencing to Macrogen, South Korea.Detection of malaria parasitesPlasmodium falciparum sporozoites in individual mosquitoes (head/thorax) were detected by analyzing high resolution melting (HRM) profiles generated from real time PCR products of non-coding mitochondrial sequence (ncMS)37. A P. falciparum DNA from National Institute for Biological Standards and Control (NIBSC; London, UK) was used as a reference positive control. PCR was carried out in a 10 µl volume consisting of 2 µl of 5X Evagreen HRM Master Mix (Solis BioDyne, Estonia), 1 µl of DNA template and 10 µM of each primer. PCR cycling conditions were initial denaturation for 15 min at 95 °C followed by 40 cycles of denaturation at 95 °C for 20 s, annealing at 61 °C for 15 s and extension at 72 °C for 20 s followed by final extension at 72 °C for 7 min. A fraction of RT-PCR-HRM positive samples were further analyzed using conventional PCR in a 10 µl volume consisting of 2 µl of 5X HOT FIREPol Blend Master Mix Ready to Load (Solis BioDyne, Estonia), 1 µl of DNA template and 10 µM of each primer. The cycling conditions comprised initial denaturation for 15 min at 95 °C followed by 40 cycles of denaturation at 95 °C for 20 s, annealing at 61 °C for 15 s and extension at 72 °C for 20 s followed by final extension at 72 °C for 7 min. PCR product of samples positive by RT-PCR were purified using ExoSAP- IT (USB Corporation, Cleveland, OH, USA) and outsourced for sequencing to Macrogen, South Korea. All sporozoite-positive mosquitoes were molecularly identified to species by PCR of the ITS2 region as described above.Genotyping for L119F-GSTe2 mutation and sequencingTwo outer and two inner primers in a PCR assay were used to genotype the L119F-GSTe2 mutations that confer resistance of An. funestus mosquitoes to pyrethroids/DDT19 as described previously28. Thus, only An. funestus s.l. was screened using this assay. Briefly, PCR in a 15 µl reaction volume consisted of 10 µM of each primer, 3 µl of 5X HOT FIREPol Blend Master Mix Ready to Load (Solis BioDyne, Estonia), and 2 µl of DNA template. The cycling conditions were initial denaturation at 95 °C for 15 min, followed by 40 cycles of denaturation at 95 °C for 30 s, annealing at 59 °C for 30 s and extension at 72 °C for 40 s and final extension at 72 °C for 7 min. Amplicons were resolved in a 1.5% agarose gel stained with ethidium bromide (Sigma-Aldrich, GmbH, Germany) against a 1 Kb DNA ladder (HyperLadder, Bioline, London, UK). The amplicons were scored as either homozygous susceptible (SS) at 312 bp, homozygous resistant (RR) at 523 bp or heterozygous (RS) when both bands were visualized.Representative GSTe2 allele positive samples were sequenced for the GSTe2 gene using the Gste2F and Gste2R primers as described previously38. PCR comprised a reaction volume of 15 µl in MyTaq DNA Polymerase Kit (Bioline, London, UK) containing 10 µM of each primer, 5X My Taq reaction buffer, 2 µl of My taq DNA polymerase and 1 µl of DNA template. PCR conditions were: initial denaturation of 5 min at 95 °C, followed by 30 cycles of 94 °C for 30 s, 58 °C for 30 s and 72 °C for 1 min, with a final extension at 72 °C for 10 min. Cleaning and sequencing of amplicons were performed as described above.Sequence and polymorphism analysisSequences (mosquito, P. falciparum, GSTe2) were viewed and cleaned in Geneious Prime39 and queried in GenBank using Basic Local Alignment Search Tool (BLastn). Parasite sequences were assigned as P. falciparum after  > 98% percentage identity. MAFFT in Geneious Prime39 was used to perform multiple sequence alignments with default parameters. Maximum likelihood (ML) trees were inferred for mosquito ITS2 sequences using the best fit model of sequence evolution with nodal support for different groupings evaluated through 1000 bootstrap replications. GSTe2 gene polymorphism analysis was performed in Geneious Prime and ML tree reconstructed from MAFFT alignment using PhyML v. 2.2.4. Haplotype distribution network was constructed using Templeton-Crandall Sing (TCS) program v. 1.2140.Statistical analysisRelative abundance was used to estimate the outdoor composition of the anopheline mosquitoes. Daily counts of female mosquito/trap/night for An. funestus s.l. and An. gambiae s.l. were compared for each area using generalized linear models (GLM) with negative binomial error structure based on best-fit model residuals. The mean catches/trap/night was computed for each of the species complexes. The P. falciparum sporozoite infection rates (Pfsp) were expressed as the number of positive specimens of the total number of specimens examined. The distribution of L119F-GSTe2 mutations was assessed by determining allelic frequencies in different species. Infection status among the resistant mosquitoes was compared using the Fisher’s Exact Test. Data were analyzed using R v 4.1.0 software at 95% confidence limit.Ethical considerationsEthical review and approval of the study was granted by the Scientific and Ethical Review Unit (SERU) of the Kenya Medical Research Institute (KEMRI) (Protocol No. SSC 2787). Prior to data collection, the purpose of the study, procedures and associated benefits/risks were provided to the local leadership at county and community levels. Additionally, informed verbal consent to trap mosquitoes around homesteads was obtained from household heads. More

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    Indigenous oyster fisheries persisted for millennia and should inform future management

    Cooke, S. J. et al. Knowledge co-production: A pathway to effective fisheries management, conservation, and governance. Fisheries 46, 89–97 (2021).Article 

    Google Scholar 
    Kobluk, H. M. et al. Indigenous knowledge of key ecological processes confers resilience to a small-scale kelp fishery. People Nat. 3, 723–739 (2021).Article 

    Google Scholar 
    Lee, L. C. et al. Drawing on indigenous governance and stewardship to build resilient coastal fisheries: People and abalone along Canada’s northwest coast. Mar. Policy 109, 103701 (2019).Article 

    Google Scholar 
    Reid, A. J. et al. “Two-Eyed Seeing”: An Indigenous framework to transform fisheries research and management. Fish. Fish. 22, 243–261 (2021).Article 

    Google Scholar 
    Toniello, G., Lepofsky, D., Lertzman-Lepofsky, G., Salomon, A. K. & Rowell, K. 11,500 y of human–clam relationships provide long-term context for intertidal management in the Salish Sea, British Columbia. Proc. Natl Acad. Sci. 116, 22106–22114 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ahn, J. E. & Ronan, A. D. Development of a model to assess coastal ecosystem health using oysters as the indicator species. Estuar., Coast. Shelf Sci. 233, 106528 (2020).CAS 
    Article 

    Google Scholar 
    Skilbeck, C. G., Heap, A. D. & Woodroffe, C. D. Geology and sedimentary history of modern estuaries. in Applications of Paleoenvironmental Techniques in Estuarine Studies (eds. Weckström, K., Saunders, K. M., Gell, P. A. & Skilbeck, C. G.) 45–74 (Springer Netherlands, 2017). https://doi.org/10.1007/978-94-024-0990-1_3.Durham, S. R., Gillikin, D. P., Goodwin, D. H. & Dietl, G. P. Rapid determination of oyster lifespans and growth rates using LA-ICP-MS line scans of shell Mg/Ca ratios. Palaeogeogr., Palaeoclimatol., Palaeoecol. 485, 201–209 (2017).Article 

    Google Scholar 
    Lockwood, R. & Mann, R. A conservation palaeobiological perspective on Chesapeake Bay oysters. Philos. Trans. R. Soc. B 374, 20190209 (2019).CAS 
    Article 

    Google Scholar 
    Rick, T. C. et al. Millennial-scale sustainability of the Chesapeake Bay native American oyster fishery. Proc. Natl Acad. Sci. 113, 6568–6573 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Thompson, V. D. et al. Ecosystem stability and Native American oyster harvesting along the Atlantic Coast of the United States. Sci. Adv. 6, eaba9652 (2020).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Zimmt, J. B., Lockwood, R., Andrus, C. F. T. & Herbert, G. S. Sclerochronological basis for growth band counting: A reliable technique for life-span determination of Crassostrea virginica from the mid-Atlantic United States. Palaeogeogr. Palaeoclimatol. Palaeoecol. 516, 54–63 (2019).Article 

    Google Scholar 
    Alleway, H. K. & Connell, S. D. Loss of an ecological baseline through the eradication of oyster reefs from coastal ecosystems and human memory. Conserv Biol. 29, 795–804 (2015).PubMed 
    Article 

    Google Scholar 
    Beck, M. W. et al. Oyster reefs at risk and recommendations for conservation, restoration, and management. Bioscience 61, 107–116 (2011).Article 

    Google Scholar 
    Kirby, M. X. Fishing down the coast: Historical expansion and collapse of oyster fisheries along continental margins. Proc. Natl Acad. Sci. 101, 13096 (2004).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lotze, H. K. et al. Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312, 1806 (2006).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Zu Ermgassen, P. S. et al. Historical ecology with real numbers: Past and present extent and biomass of an imperilled estuarine habitat. Proc. R. Soc. B: Biol. Sci. 279, 3393–3400 (2012).Article 

    Google Scholar 
    Carranza, A., Defeo, O. & Beck, M. Diversity, conservation status and threats to native oysters (Ostreidae) around the Atlantic and Caribbean coasts of South America. Aquat. Conserv.: Mar. Freshw. Ecosyst. 19, 344–353 (2009).Article 

    Google Scholar 
    Pluckhahn, T. J. & Thompson, V. D. Woodland-period mound building as historical tradition: Dating the mounds and monuments at Crystal River (8CI1). J. Archaeological Sci.: Rep. 15, 73–94 (2017).Article 

    Google Scholar 
    Waselkov, G. A. Shellfish gathering and shell midden archaeology. Adv. Archaeol. Method Theory 10, 93–210 (1987).Article 

    Google Scholar 
    McNiven, I. J. Ritualized middening practices. J. Archaeol. Method Theory 20, 552–587 (2013).Article 

    Google Scholar 
    Hawkes, A. D. et al. Relative sea-level change in northeastern Florida (USA) during the last ~8.0 ka. Quat. Sci. Rev. 142, 90–101 (2016).ADS 
    Article 

    Google Scholar 
    Kelley, J. T., Belknap, D. F. & Claesson, S. Drowned coastal deposits with associated archaeological remains from a sea-level “slowstand”: Northwestern Gulf of Maine, USA. Geology 38, 695–698 (2010).ADS 
    Article 

    Google Scholar 
    Khan, N. S. et al. Drivers of Holocene sea-level change in the Caribbean. Quat. Sci. Rev. 155, 13–36 (2017).ADS 
    Article 

    Google Scholar 
    Love, R. et al. The contribution of glacial isostatic adjustment to projections of sea-level change along the Atlantic and Gulf coasts of North America. Earth’s Future 4, 440–464 (2016).ADS 
    Article 

    Google Scholar 
    Shugar, D. H. et al. Post-glacial sea-level change along the Pacific coast of North America. Quat. Sci. Rev. 97, 170–192 (2014).ADS 
    Article 

    Google Scholar 
    Dougherty, A. J. et al. Redating the earliest evidence of the mid-Holocene relative sea-level highstand in Australia and implications for global sea-level rise. PLoS ONE. 14, e0218430 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bailey, G. N. The role of molluscs in coastal economies: The results of midden analysis in Australia. J. Archaeol. Sci. 2, 45–62 (1975).Article 

    Google Scholar 
    Habu, J., Matsui, A., Yamamoto, N. & Kanno, T. Shell midden archaeology in Japan: Aquatic food acquisition and long-term change in the Jomon culture. Quat. Int. 239, 19–27 (2011).Article 

    Google Scholar 
    Hale, J. C. et al. Submerged landscapes, marine transgression and underwater shell middens: Comparative analysis of site formation and taphonomy in Europe and North America. Quat. Sci. Rev. 258, 106867 (2021).Article 

    Google Scholar 
    Erlandson, J. M. et al. Shellfish, geophytes, and sedentism on Early Holocene Santa Rosa Island, Alta California, USA. J. Isl. Coast. Archaeol. 15, 504–524 (2020).Article 

    Google Scholar 
    Rick, T. C. Early to Middle Holocene estuarine shellfish collecting on the islands and mainland coast of the Santa Barbara Channel, California, USA. Open Quaternary 6, 9 (2020).Sanger, D. & Sanger, M. J. Boom and bust on the river: The story of the Damariscotta oyster shell heaps. Archaeol. East. North Am. 14, 65–78 (1986).
    Google Scholar 
    Moss, M. L. Shellfish gender, and status on the Northwest Coast: Reconciling archaeological, ethnographic, and ethnohistoric records of the Tlingit. Am. Anthropologist 95, 631–652 (1993).Article 

    Google Scholar 
    Cannon, A., Burchell, M. & Bathurst, R. Trends and strategies in shellfish gathering on the Pacific Northwest Coast of North America. in Early Human Impact on Megamolluscs (eds. Antczak, A. & Cipriani, R.) 7–22 (Archaeopress, 2008).Grier, C., Angelbeck, B. & McLay, E. Terraforming and monumentality as long-term social practice in the Salish Sea region of the Northwest Coast of North America. Hunt. Gatherer Res. 3, 107–132 (2017).Article 

    Google Scholar 
    Pluckhahn, T. J. & Thompson, V. D. New Histories of Village Life at Crystal River. (University Press of Florida, 2018).Thompson, V. D. et al. Ancient engineering of fish capture and storage in southwest Florida. Proc. Natl Acad. Sci. 117, 8374–8381 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Sassaman, K. E. Complex hunter–gatherers in evolution and history: A North American perspective. J. Archaeol. Res. 12, 227–280 (2004).Article 

    Google Scholar 
    Luby, E. M. & Gruber, M. F. The dead must be fed: Symbolic meanings of the shellmounds of the San Francisco Bay area. Camb. Archaeol. J. 9, 95–108 (1999).Article 

    Google Scholar 
    Lightfoot, K. G. & Luby, E. M. Mound building by California hunter-gatherers. in The Oxford Handbook of North American Archaeology (ed. Pauketat, T.) 212–223 (Oxford University Press, 2012).Smith, A. D. T. Archaeological expressions of Holocene cultural and environmental change in coastal Southeast Queensland. (The University of Queensland, 2016).Reeder-Myers, L., Rick, T., Lowery, D., Wah, J. & Henkes, G. Human ecology and coastal foraging at Fishing Bay, Maryland, USA. J. Ethnobiol. 36, 595–616 (2016).Article 

    Google Scholar 
    Petrie, C. C. Tom Petrie’s reminiscences of Early Queensland (dating from 1837). (Watson, Ferguson & Company, 1904).Eipper, C. Statement of the Origin, Condition and Prospects, of the German Mission to the Aborigines at Moreton Bay, etc. (James Reading, 1841).Watkins, G. Notes on the Aboriginals of Stradbroke and Moreton Islands. Proc. R. Soc. Qld. 8, 40–50 (1891).
    Google Scholar 
    Ross, A. & with members of the Quandamooka Aboriginal Land Council. Aboriginal approaches to cultural heritage management: A Quandamooka case study. in Australian Archaeology ’95: Proceedings of the 1995 Australian Archaeological Association Annual Conference (eds. Ulm, S., Lilley, I. & Ross, A.) vol. Tempus 6 107–112 (Anthropology Museum, University of Queensland, 1996).Jenkins, J. A. & Gallivan, M. D. Shell on earth: Oyster harvesting, consumption, and deposition practices in the Powhatan Chesapeake. J. Isl. Coast. Archaeol. 15, 384–406 (2020).Article 

    Google Scholar 
    Hatch, M. B. A. & Wyllie-Echeverria, S. Historic distribution of Ostrea lurida (Olympia oyster) in the San Juan Archipelago. Wash. State Tribal Coll. Univ. Res. J. 1, 38–45 (2016).
    Google Scholar 
    Swanton, J. R. Social Organization and Social Usages of the Indians of the Creek Confederacy. (Bureau of American Ethnology, 1928).Hening, W. W. The Statutes at Large of Virginia. (1809).Wharton, J. The Bounty of the Chesapeake: Fishing in Colonial Virginia. (Virginia 350th Anniversary Celebration Corporation, 1957).Denys, N. Description géographique et historique des Costes de l’Amérique Septentrionale. Avec l’Histoire naturelle du Pais. (Chez Claude Barbin, 1672).Nicolar, J. The Life and Traditions of the Red Man. (Duke University Press, 2007 Print, 1893).Speck, F. G. Penobscot Man: The Life History of a Forest Tribe in Maine. (University of Pennsylvania Press, 1940).Washburn, K. Passamaquoddy tribe conducts oyster project. Bangor Daily News (1979).Kennedy, V. S. Shifting Baselines in the Chesapeake Bay: An Environmental History. (Johns Hopkins University Press, 2018).de Charlevoix, P. F. X. Journal of a Voyage to North America, Vollume II. Translated by Louise Phelps Kellogg. (The Caxton Club, 1923).Ingersoll, E. The Oyster Industry. (United States Bureau of Fisheries, United States Census Office, Government Printing Office, 1881).Brice, J. J. Report on the fish and fisheries of the coastal waters of Florida. in Report of the Commissioner for the Year Ending June 30, 1896 263–242 (U.S. Commission of Fish and Fisheries, U.S. Government Printing Office, 1896).Blake, B. & Zu Ermgassen, P. S. E. The history and decline of Ostrea lurida in Willapa Bay, Washington. J. Shellfish Res. 34, 273–280 (2015).Article 

    Google Scholar 
    Thurstan, R. H. et al. Charting two centuries of transformation in a coastal social-ecological system: A mixed methods approach. Global Environmental Change 61, 102058 (2020).Schulte, D. M. History of the Virginia oyster fishery, Chesapeake Bay, USA. Front. Mar. Sci. 4, 127 (2017).Fletcher, M.-S., Hamilton, R., Dressler, W. & Palmer, L. Indigenous knowledge and the shackles of wilderness. Proc. Natl Acad. Sci. 118, e2022218118 (2021).Ross, A., Coghill, S. & Coghill, B. Discarding the evidence: The place of natural resources stewardship in the creation of the Peel Island Lazaret Midden, Moreton Bay, southeast Queensland. Quat. Int. 385, 177–190 (2015).Article 

    Google Scholar 
    Reeder-Myers, L. A. & Rick, T. C. Kayak surveys in estuarine environments: addressing sea level rise and climate change. Antiquity 93, 1040–1051 (2019).Article 

    Google Scholar 
    Savarese, M., Walker, K. J., Stingu, S., Marquardt, W. H. & Thompson, V. The effects of shellfish harvesting by aboriginal inhabitants of Southwest Florida (USA) on productivity of the eastern oyster: Implications for estuarine management and restoration. Anthropocene 16, 28–41 (2016).Article 

    Google Scholar 
    Lulewicz, I. H., Thompson, V. D., Cramb, J. & Tucker, B. Oyster paleoecology and native American subsistence practices on Ossabaw Island, Georgia, USA. J. Archaeol. Sci.: Rep. 15, 282–289 (2017).
    Google Scholar 
    Hesterberg, S. G. et al. Prehistoric baseline reveals substantial decline of oyster reef condition in a Gulf of Mexico conservation priority area. Biol. Lett. 16, 20190865 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Cannarozzi, N. R. & Kowalewski, M. Seasonal oyster harvesting recorded in a Late Archaic period shell ring. PloS ONE. 14, e0224666 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Cook-Patton, S. C., Weller, D., Rick, T. C. & Parker, J. D. Ancient experiments: Forest biodiversity and soil nutrients enhanced by Native American middens. Landsc. Ecol. 29, 979–987 (2014).Article 

    Google Scholar 
    Stalter, R. & Kincaid, D. The vascular flora of five Florida shell middens. J. Torre. Botanical Soc. 131, 93–103 (2004).Article 

    Google Scholar 
    Kirby, M. X. & Miller, H. M. Response of a benthic suspension feeder (Crassostrea virginica Gmelin) to three centuries of anthropogenic eutrophication in Chesapeake Bay. Estuar. Coast. Shelf Sci. 62, 679–689 (2005).ADS 
    Article 

    Google Scholar 
    Suttles, W. Variation in habitat and culture on the Northwest Coast. in Coastal Salish Essays 26–44 (University of Washington Press, 1987).Bliege Bird, R. & Nimmo, D. Restore the lost ecological functions of people. Nat. Ecol. Evolution 2, 1050–1052 (2018).Article 

    Google Scholar 
    Berkes, F. Indigenous ways of knowing and the study of environmental change. J. R. Soc. N.Z. 39, 151–156 (2009).Article 

    Google Scholar 
    Tengö, M., Malmer, P., Elmqvist, T. & Brondizio, E. S. A Framework for Connecting Indigenous, Local and Scientific Knowledge Systems. (2012).Ellis, E. C. et al. People have shaped most of terrestrial nature for at least 12,000 years. Proc. Natl Acad. Sci.118, e2023483118 (2021).Roberts, P. et al. Reimagining the relationship between Gondwanan forests and Aboriginal land management in Australia’s “Wet Tropics”. Iscience 24, 102190 (2021).Ogburn, D. M., White, I. & McPhee, D. P. The disappearance of oyster reefs from eastern Australian estuaries—impact of colonial settlement or mudworm invasion? Coast. Manag. 35, 271–287 (2007).Article 

    Google Scholar 
    Diggles, B. K. Historical epidemiology indicates water quality decline drives loss of oyster (Saccostrea glomerata) reefs in Moreton Bay, Australia. N.Z. J. Mar. Freshw. Res. 47, 561–581 (2013).CAS 
    Article 

    Google Scholar 
    Pritchard, C., Shanks, A., Rimler, R., Oates, M. & Rumrill, S. The Olympia oyster Ostrea lurida: Recent advances in natural history, ecology, and restoration. J. Shellfish Res. 34, 259–271 (2015).Article 

    Google Scholar 
    Trimble, A. C., Ruesink, J. L. & Dumbauld, B. R. Factors preventing the recovery of a historically overexploited shellfish species, Ostrea lurida Carpenter 1864. J. Shellfish Res. 28, 97–106 (2009).Article 

    Google Scholar 
    White, J., Ruesink, J. L. & Trimble, A. C. The nearly forgotten oyster: Ostrea lurida Carpenter 1864 (Olympia oyster) history and management in Washington State. J. Shellfish Res. 28, 43–49 (2009).Article 

    Google Scholar 
    Harding, J. M., Spero, H. J., Mann, R., Herbert, G. S. & Sliko, J. L. Reconstructing early 17th century estuarine drought conditions from Jamestown oysters. Proc. Natl Acad. Sci. 107, 10549–10554 (2010).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Mann, R., Harding, J. M. & Southworth, M. J. Reconstructing pre-colonial oyster demographics in the Chesapeake Bay, USA. Estuar., Coast. Shelf Sci. 85, 217–222 (2009).ADS 
    Article 

    Google Scholar 
    Bayne, B. L. Biology of Oysters. (Elsevier Science & Technology, 2017).Galtsoff, P. S. The American Oyster Crassostrea virginica Gmelin. (United States Government Printing Office, 1964).Kennedy, V. S., Newell, R. I. E. & Eble, A. F. The Eastern Oyster: Crassostrea virginica. (University of Maryland Sea Grant Publications, 1996).Grabowski, J. H., Powers, S. P., Peterson, C. H., Gaskill, D. & Summerson, H. C. Growth and survivorship of non-native (Crassostrea gigas and Crassostrea ariakensis) versus native eastern (Crassostrea virginica) oysters. J. Shellfish Res. 23, 781–793 (2004).
    Google Scholar 
    Shumway, S. Natural environmental factors. in The eastern oyster Crassostrea virginica (eds. Kennedy, V., Newell, R. & Eble, A.) 467–513 (Maryland Sea Grant, 1996).Lyman, R. L. Paleoenvironmental reconstruction from faunal remains: Ecological basics and analytical assumptions. J. Archaeol. Res. 25, 315–371 (2017).MathSciNet 
    Article 

    Google Scholar 
    Claasen, C. Shells. (Cambridge University Press, 1990).Giovas, C. M. The shell game: Analytic problems in archaeological mollusc quantification. J. Archaeol. Sci. 36, 1557–1564 (2009).Article 

    Google Scholar 
    Peltier, W. R., Argus, D. F. & Drummond, R. Space geodesy constrains ice age terminal deglaciation: The global ICE-6G_C (VM5a) model: Global Glacial Isostatic Adjustment. J. Geophys. Res.: Solid Earth 120, 450–487 (2015).ADS 
    Article 

    Google Scholar  More

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    New cyanobacterial genus Argonema is hidding in soil crusts around the world

    Argonema gen. nov. Skoupý et Dvořák.Type species: Argonema galeatum.Morphology: Filamentous cyanobacterium, colonies macroscopic, growing in round bulbs and tufts. The filaments are dark green to blue-green, grey-green or brown-green in color. Cells are wider than they are long. Filaments sheathed, sheaths are colorless to light brown, distinct, and variable in length. The filament can protrude from the sheath or the sheath can exceed filament. Trichomes are cylindrical, not attenuated to slightly attenuated towards the end, slightly or not constricted at cell walls. The apical cell can be concave, dark brown, purple-brown to almost black. Cell content often granulated. Necridic cells present, reproduction by hormogonia. The morphological description was based on both culture and fresh material.Etymology: The genus epithet (Argonema) is derived from greek Argo – slow, latent (αργός) and nema – thread (νήμα).A. galeatum sp. nov. Skoupý et Dvořák.Morphology: The cells of A. galeatum are 6.5–9.1 µm (mean 7.81 µm) wide and 1.1–2.5 µm (mean 1.83 µm) long (Figs. 1–5). Filaments are straight, blue-green to gray-green in color. The sheaths are colorless to light brown, distinct, and variable in length. The filament can protrude from the sheath or the sheath can exceed filament. No true branching was observed. Trichomes are cylindrical, not attenuated or slightly attenuated towards the end, slightly or not constricted at cell walls. Some filaments have a concave apical cell that is dark brown, purple-brown to almost black (Fig. 11b). Cell content often granulated. Reproduction by necridic cells and subsequent breaking of the filaments into hormogonia (Fig. 11a,c). The morphological description was based on both culture and fresh material.Figures 1-8Microphotographs of Argonema galeatum (Figs 1–5) and Argonema antarcticum (Figs. 6–8) Trichomes of A. galeatum appear more straight (Fig 2), while trichomes of A. antarcticum form waves (Fig 6) and loops (Fig 7). Scale = 10 µm, wide arrow = necridic cells, arrowhead = granules, asterisk = colored apical cell, circle = empty sheath.Full size imageFigures 9 and 10Histograms of cell dimensions constructed using PAST software. Fig. 9 – Histogram of cell width frequencies in A. galeatum (blue) and A. antarcticum (red). Fig. 10 – Histogram of cell length frequencies in A. galeatum (blue) and A. antarcticum (red).Full size imageHolotype: 38,057, Herbarium of the Department of Botany (OL), Palacký University Olomouc, Czech Republic.Reference strain: Argonema galeatum A003/A1.Type locality: James Ross Island, Western Antarctica, 63.80589S, 57.92147 W.Habitat: Well-developed soil crust.Etymology: Species epithet A. galeatum was derived from latin galea – helmet.A. antarcticum sp. nov. Skoupý et Dvořák.Morphology: The cells are 7.6–9.2 µm (mean 8.52 µm) wide and 1.2–2.8 µm (mean 1.72 µm) long (Figs. 5–8). Filaments are wavy, gray-green to brown-green in color. The sheaths are colorless to light brown, distinct, and variable in length. The filament can protrude from the sheath or the sheath can exceed filament. No true branching was observed. Trichomes are cylindrical, not attenuated or slightly attenuated towards the end with a concave apical cell, slightly or not constricted at cell walls (Fig. 11d). Necridic cells present (Fig. 11e), reproduction by hormogonia. The morphological description was based on both culture and fresh material.Holotype: 38,058, Herbarium of the Department of Botany (OL), Palacký University, Olomouc, Czech Republic.Reference strain: Argonema antarcticum A004/B2.Type locality: James Ross Island, Western Antarctica, 63.89762S, 57.79743 W.Habitat: Well-developed soil crust.Etymology: Species epithet A. antarcticum was derived from the original sampling site.Morphological variabilityWe used light microscopy to assess the morphology of Argonema from soil crust samples and cultured strains. Argonema is morphologically similar to other Oscillatoriales, such as Lyngbya, Phormidium, and Oscillatoria. In culture, the morphology of A. galeatum and A. antarcticum differed slightly. Filaments of A. antarcticum are wider than cells of A. galeatum, averaging at 8.52 µm (A. galeatum – 7.81 µm). The average cell width/length ratio is 4.54 for A.galeatum and 4.89 for A. antarcticum. The cell width was significantly different between the two species (Nested ANOVA, p  More

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    Sabertooth carcass consumption behavior and the dynamics of Pleistocene large carnivoran guilds

    Turner, A. & Antón, M. The Big Cats and Their Fossil Relatives (Columbia University Press, 1997).
    Google Scholar 
    Werdelin, L., Yamaguchi, N., Johnson, W. E. & O’Brien, S. J. Phylogeny and evolution of cats (Felidae). In Biology and Conservation of Wild Felids (eds MacDonald, D. W. & Loveridge, A. J.) 59–82 (Oxford University Press, 2011).
    Google Scholar 
    Antón, M. Sabertooth (Indiana University Press, 2013).
    Google Scholar 
    Ewer, R. F. The Carnivores (Cornell University Press, 1973).
    Google Scholar 
    Terborgh, J. W. et al. Ecological meltdown in predator-free forest fragments. Science 294, 1923–1926. https://doi.org/10.1126/science.1064397 (2001).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Sinclair, A. R. E., Mduma, S. & Brashares, J. S. Patterns of predation in a diverse predator–prey system. Nature 425, 288–290. https://doi.org/10.1038/nature01934 (2003).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Estes, J. A. et al. Trophic downgrading of planet Earth. Science 333, 301–306 (2011).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Ripple, W. J. & Van Valkenburgh, B. Linking top-down forces to the Pleistocene megafaunal extinctions. Bioscience 60, 516–526. https://doi.org/10.1525/bio.2010.60.7.7 (2010).Article 

    Google Scholar 
    Van Valkenburgh, B., Hayward, M. W., Ripple, W. J., Meloro, C. & Roth, V. L. The impact of large terrestrial carnivores on Pleistocene ecosystems. Proc Natl Acad Sci USA 113, 862–867. https://doi.org/10.1073/pnas.1502554112 (2016).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Lewis, M. E. Carnivoran paleoguilds of Africa: implications for hominid food procurement strategies. J. Hum. Evol. 32, 257–288. https://doi.org/10.1006/jhev.1996.0103 (1997).CAS 
    Article 
    PubMed 

    Google Scholar 
    Lewis, M. E. The postcranial morphology of Smilodon. In Smilodon: The Iconic Sabertooth (eds Werdelin, L. et al.) 171–195 (Johns Hopkins University Press, 2018).
    Google Scholar 
    Antón, M., Galobart, A. & Turner, A. Co-existence of scimitar-toothed cats, lions and hominins in the European Pleistocene. Implications of the post-cranial anatomy of Homotherium latidens (Owen) for comparative palaeoecology. Q. Sci. Rev. 24, 1287–1301. https://doi.org/10.1016/j.quascirev.2004.09.008 (2005).ADS 
    Article 

    Google Scholar 
    Hartstone-Rose, A. & Wahl, S. Using radii-of-curvature for the reconstruction of extinct South African carnivoran masticatory behavior. C.R. Palevol 7, 629–643. https://doi.org/10.1016/j.crpv.2008.09.015 (2008).Article 

    Google Scholar 
    Andersson, K., Norman, D. & Werdelin, L. Sabretoothed carnivores and the killing of large prey. PLoS ONE 6, e24971. https://doi.org/10.1371/journal.pone.0024971 (2011).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Van Valkenburgh, B. & Hertel, F. Tough times at La Brea: tooth breakage in large carnivores of the Late Pleistocene. Science 261, 456–459 (1993).ADS 
    Article 

    Google Scholar 
    DeSantis, L. R. G., Schubert, B. W., Scott, J. R. & Ungar, P. S. Implications of diet for the extinction of saber-toothed cats and American lions. PLoS ONE 7, e52453. https://doi.org/10.1371/journal.pone.0052453 (2012).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bocherens, H. et al. Paleobiology of sabretooth cat Smilodon populator in the Pampean Region (Buenos Aires Province, Argentina) around the Last Glacial Maximum: insights from carbon and nitrogen stable isotopes in bone collagen. Palaeogeogr. Palaeoclimatol. Palaeoecol. 449, 463–474. https://doi.org/10.1016/j.palaeo.2016.02.017 (2016).Article 

    Google Scholar 
    DeSantis, L. R. G. et al. Causes and consequences of Pleistocene megafaunal extinctions as revealed from Rancho La Brea mammals. Curr. Biol. 29, 2488-2495.e2. https://doi.org/10.1016/j.cub.2019.06.059 (2019).CAS 
    Article 
    PubMed 

    Google Scholar 
    DeSantis, L. R. G., Feranec, R. S., Antón, M. & Lundelius, E. L. Dietary ecology of the scimitar-toothed cat Homotherium serum. Curr. Biol. 31, 1–8. https://doi.org/10.1016/j.cub.2021.03.061 (2021).CAS 
    Article 

    Google Scholar 
    Christiansen, P. & Adolfssen, J. S. Osteology and ecology of Megantereon cultridens SE311 (Mammalia; Felidae; Machairodontinae), a sabrecat from the Late Pliocene—Early Pleistocene of Senéze, France. Zool. J. Linn. Soc. 151, 833–884 (2007).Article 

    Google Scholar 
    Van Valkenburgh, B. Predation in sabre-tooth cats. In Palaeobiology II (eds Briggs, D. E. G. & Crowther, P. R.) 420–423 (Wiley, 2001). https://doi.org/10.1002/9780470999295.ch101.Chapter 

    Google Scholar 
    DeSantis, L. R. G. Dietary ecology of Smilodon. In Smilodon: The Iconic Sabertooth (eds Werdelin, L. et al.) 153–170 (Johns Hopkins University Press, 2018).
    Google Scholar 
    Palmqvist, P., Torregrosa, V., Pérez-Claros, J. A., Martínez-Navarro, B. & Turner, A. A re-evaluation of the diversity of Megantereon (Mammalia, Carnivora, Machairodontinae) and the problem of species identification in extinct carnivores. J. Vertebr. Paleontol. 27, 160–175. https://doi.org/10.1671/0272-4634(2007)27[160:AROTDO]2.0.CO;2 (2007).Article 

    Google Scholar 
    Van Valkenburgh, B. & Ruff, C. B. Canine tooth strength and killing behaviour in large carnivores. J. Zool. 212, 379–397 (1987).Article 

    Google Scholar 
    Gittleman, J. L. Carnivore body size: ecological and taxonomic correlates. Oecologia 67, 540–554. https://doi.org/10.1007/BF00790026 (1985).ADS 
    Article 
    PubMed 

    Google Scholar 
    Hemmer, H. Saber-tooth cats and cave lions—from fossils to felid performance and former living communities. In Late Neogene and Quaternary Biodiversity and Evolution: Regional Developments and Interregional Correlations, Courier Forschungsinstitut Senckenberg (eds Kahlke, R.-D. et al.) 1–12 (E. Schweizerbart’sche Verlagsbuchhandlung, 2007).
    Google Scholar 
    Domingo, L., Domingo, M. S., Koch, P. L., Morales, J. & Alberdi, M. T. Carnivoran resource and habitat use in the context of a Late Miocene faunal turnover episode. Palaeontology 60, 461–483. https://doi.org/10.1111/pala.12296 (2017).Article 

    Google Scholar 
    Marean, C. W. & Ehrhardt, C. L. Paleoanthropological and paleoecological implications of the taphonomy of a sabertooth’s den. J. Hum. Evol. 29, 515–547 (1995).Article 

    Google Scholar 
    Spencer, L. M., Van Valkenburgh, B. & Harris, J. M. Taphonomic analysis of large mammals recovered from the Pleistocene Rancho La Brea tar seeps. Paleobiology 29, 561–575. https://doi.org/10.1666/0094-8373(2003)029%3c0561:TAOLMR%3e2.0.CO;2 (2003).Article 

    Google Scholar 
    Chahud, A. Occurrence of the sabretooth cat Smilodon populator (Felidae, Machairodontinae) in the Cuvieri cave, eastern Brazil. Palaeontol. Electron. 23, a24. https://doi.org/10.26879/1056 (2020).Article 

    Google Scholar 
    Prevosti, F. J. & Martín, F. M. Paleoecology of the mammalian predator guild of southern Patagonia during the latest Pleistocene: ecomorphology, stable isotopes, and taphonomy. Quat. Int. 305, 74–84. https://doi.org/10.1016/j.quaint.2012.12.039 (2013).Article 

    Google Scholar 
    Lindsey, E. L. & Seymour, K. L. “Tar Pits” of the western neotropics: paleoecology, taphonomy, and mammalian biogeography. In La Brea and Beyond: The Palaeontology of Asphalt-Preserved Biotas (ed. Harris, J. M.) 111–123 (Natural History Museum of Los Angeles County, 2015).
    Google Scholar 
    Hulbert, R. C. The Fossil Vertebrates of Florida (University of Florida Press, 2001).
    Google Scholar 
    Domingo, M. S., Alberdi, M. T., Azanza, B., Silva, P. G. & Morales, J. Origin of an assemblage massively dominated by carnivorans from the Miocene of Spain. PLoS ONE 8, e63046. https://doi.org/10.1371/journal.pone.0063046 (2013).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Brain, C. K. The Hunters or the Hunted: An Introduction to African Cave Taphonomy (University of Chicago Press, 1981).
    Google Scholar 
    Palmqvist, P., Martínez-Navarro, B. & Arribas, A. Prey selection by terrestrial carnivores in a lower Pleistocene paleocommunity. Paleobiology 22, 514–534. https://doi.org/10.1017/S009483730001650X (1996).Article 

    Google Scholar 
    Morgan, G. S. & Hulbert, R. C. Overview of the geology and vertebrate biochronology of the Leisey Shell Pit Local Fauna, Hillsborough County, Florida. Bull. Am. Mus. Nat. Hist. 37, 1–92 (1995).
    Google Scholar 
    Martin, L. D., Babiarz, J. P., Naples, V. L. & Hearst, J. Three ways to be a saber-toothed cat. Naturwissenschaften 87, 41–44 (2000).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    M. Domínguez-Rodrigo, C.P. Egeland, T.R. Pickering, Equifinality in carnivore tooth marks and the extended concept of archaeological palimpsests: implications for models of passive scavenging by early hominid. In: Breathing Life into Fossils: Taphonomic Studies in Honor of C.K. (Bob) Brain, Stone Age Institute Press, Gosport, Indiana, 2007, pp. 255–267.Gidna, A. O., Kisui, B., Mabulla, A. Z. P., Musiba, C. & Domínguez-Rodrigo, M. An ecological neo-taphonomic study of carcass consumption by lions in Tarangire National Park (Tanzania) and its relevance for human evolutionary biology. Quat. Int. 322–323, 167–180. https://doi.org/10.1016/j.quaint.2013.08.059 (2014).Article 

    Google Scholar 
    Gidna, A. O., Domínguez-Rodrigo, M. & Pickering, T. R. Patterns of bovid long limb bone modification created by wild and captive leopards and their relevance to the elaboration of referential frameworks for paleoanthropology. J. Archaeol. Sci. Rep. 2, 302–309. https://doi.org/10.1016/j.jasrep.2015.03.003 (2015).Article 

    Google Scholar 
    Yravedra, J., Lagos, L. & Bárcena, F. A taphonomic study of wild wolf (Canis lupus) modification of horse bones in northwestern Spain. J. Taphon. 9, 37–65 (2011).
    Google Scholar 
    Fosse, P. et al. Bone modification by modern wolf (Canis lupus): a taphonomic study from their natural feeding places. J. Taphon. 10, 197–217 (2012).
    Google Scholar 
    Domínguez-Rodrigo, M. & Pickering, T. R. A multivariate approach for discriminating bone accumulations created by spotted hyenas and leopards: harnessing actualistic data from East and southern Africa. J. Taphon. 8, 155–179 (2010).
    Google Scholar 
    Domínguez-Rodrigo, M., Gidna, A. O., Yravedra, J. & Musiba, C. A comparative neo-taphonomic study of felids, hyaenids and canids: an analogical framework based on long bone modification patterns. J. Taphon. 10, 151–170 (2012).
    Google Scholar 
    Gidna, A., Yravedra, J. & Domínguez-Rodrigo, M. A cautionary note on the use of captive carnivores to model wild predator behavior: a comparison of bone modification patterns on long bones by captive and wild lions. J. Archaeol. Sci. 40, 1903–1910. https://doi.org/10.1016/j.jas.2012.11.023 (2013).Article 

    Google Scholar 
    Parkinson, J. A., Plummer, T. & Hartstone-Rose, A. Characterizing felid tooth marking and gross bone damage patterns using GIS image analysis: an experimental feeding study with large felids. J. Hum. Evol. 80, 114–134. https://doi.org/10.1016/j.jhevol.2014.10.011 (2015).Article 
    PubMed 

    Google Scholar 
    Domínguez-Rodrigo, M. et al. A 3D taphonomic model of long bone modification by lions in medium-sized ungulate carcasses. Sci. Rep. 11, 4944. https://doi.org/10.1038/s41598-021-84246-1 (2021).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Arriaza, M. C. et al. Striped hyenas as bone modifiers in dual human-to-carnivore experimental models. Archaeol. Anthropol. Sci. 11, 3187–3199. https://doi.org/10.1007/s12520-018-0747-y (2019).Article 

    Google Scholar 
    Marean, C. W., Spencer, L. M., Blumenschine, R. J. & Capaldo, S. D. Captive hyaena bone choice and destruction, the Schlepp effect and Olduvai archaeofaunas. J. Archaeol. Sci. 19, 101–121. https://doi.org/10.1016/0305-4403(92)90009-R (1992).Article 

    Google Scholar 
    Woodruff, A. L. & Schubert, B. W. Seasonal denning behavior and population dynamics of the late Pleistocene peccary Platygonus compressus (Artiodactyla: Tayassuidae) from Bat Cave, Missouri. PeerJ 7, 1–18. https://doi.org/10.7717/peerj.7161 (2019).Article 

    Google Scholar 
    de Ruiter, D. J. & Berger, L. R. Leopards as taphonomic agents in dolomitic caves—implications for bone accumulations in the hominid-bearing deposits of South Africa. J. Archaeol. Sci. 27, 665–684. https://doi.org/10.1006/jasc.1999.0470 (2000).Article 

    Google Scholar 
    Domínguez-Rodrigo, M. Dinámica trófica, estrategias de consumo y alteraciones óseas en la sabana africana: resumen de un proyecto de investigación etoarqueológico (1991–1993). Trab. Prehist. 51, 15–37 (1994).Article 

    Google Scholar 
    Arriaza, M. C., Domínguez-Rodrigo, M., Yravedra, J. & Baquedano, E. Lions as bone accumulators? Paleontological and ecological implications of a modern bone assemblage from Olduvai Gorge. PLoS ONE 11, e0153797. https://doi.org/10.1371/journal.pone.0153797 (2016).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Schaller, G. B. The Serengeti Lion: A Study of Predator-Prey Relations (University of Chicago Press, 1972).
    Google Scholar 
    Brain, C. K. Some suggested procedures in the analysis of bone accumulations from southern African Quaternary sites. Ann. Transvaal Mus. 29, 1–8 (1974).
    Google Scholar 
    Christiansen, P. Phylogeny of the sabertoothed felids (Carnivora: Felidae: Machairodontinae). Cladistics 29, 543–559. https://doi.org/10.1111/cla.12008 (2013).Article 
    PubMed 

    Google Scholar 
    Rawn-Schatzinger, V. Development and eruption sequence of deciduous and permanent teeth in the saber-tooth cat Homotherium serum Cope. J. Vertebr. Paleontol. 3, 49–57. https://doi.org/10.1080/02724634.1983.10011958 (1983).Article 

    Google Scholar 
    Rawn-Schatzinger,V. The Scimitar Cat Homotherium serum Cope: Osteology, Functional Morphology, and Predatory Behavior, Illinois State Museum, Springfield, IL, 1992.White, P. A. & Diedrich, C. G. Taphonomy story of a modern African elephant Loxodonta africana carcass on a lakeshore in Zambia (Africa). Quat. Int. 276–277, 287–296 (2012).Article 

    Google Scholar 
    Haynes, G. & Klimowicz, J. Recent elephant-carcass utilization as a basis for interpreting mammoth exploitation. Quat. Int. 359–360, 19–37. https://doi.org/10.1016/j.quaint.2013.12.040 (2015).Article 

    Google Scholar 
    Biknevicius, A. R., Van Valkenburgh, B. & Walker, J. Incisor size and shape: implications for feeding behaviors in saber-toothed “cats”. J. Vertebr. Paleontol. 16, 510–521 (1996).Article 

    Google Scholar 
    Van Valkenburgh, B. Incidence of tooth breakage among large, predatory mammals. Am. Nat. 131, 291–302. https://doi.org/10.1086/284790 (1988).Article 

    Google Scholar 
    DeSantis, L. R. G. et al. Dental microwear textures of carnivorans from the La Brea Tar Pits, California, and potential extinction implications. In La Brea and Beyond: The Paleontology of Asphalt-Preserved Biotas (ed. Harris, J. M.) 37–52 (Natural History Museum of Los Angeles County, 2015).
    Google Scholar 
    Paijmans, J. L. A. et al. Evolutionary history of saber-toothed cats based on ancient mitogenomics. Curr. Biol. 27, 3330-3336.e5. https://doi.org/10.1016/j.cub.2017.09.033 (2017).CAS 
    Article 
    PubMed 

    Google Scholar 
    Antón, M., Salesa, M. J., Galobart, A. & Tseng, Z. J. The Plio-Pleistocene scimitar-toothed felid genus Homotherium Fabrini, 1890 (Machairodontinae, Homotherini): diversity, palaeogeography and taxonomic implications. Quat. Sci. Rev. 96, 259–268. https://doi.org/10.1016/j.quascirev.2013.11.022 (2014).ADS 
    Article 

    Google Scholar 
    Thompson, J. C., Carvalho, S., Marean, C. W. & Alemseged, Z. Origins of the human predatory pattern: The transition to large-animal exploitation by early hominins. Curr. Anthropol. 60, 1–23. https://doi.org/10.1086/701477 (2019).Article 

    Google Scholar 
    Plummer, T. Flaked stones and old bones: biological and cultural evolution at the dawn of technology. Yearb. Phys. Anthropol. 47, 118–164. https://doi.org/10.1002/ajpa.20157 (2004).Article 

    Google Scholar 
    Turner, A. Relative scavenging opportunities for East and South African Plio-Pleistocene hominids. J. Archaeol. Sci. 15, 327–341 (1988).Article 

    Google Scholar 
    Turner, A. The evolution of the guild of larger terrestrial carnivores during the Plio-Pleistocene in Africa. Geobios 23, 349–368 (1990).Article 

    Google Scholar 
    Turner, A. Large carnivores and earliest European hominids: changing determinants of resource availability during the Lower and Middle Pleistocene. J. Hum. Evol. 22, 109–126 (1992).Article 

    Google Scholar 
    Van Valkenburgh, B. The dog-eat-dog world of carnivores: a review of past and present carnivore community dynamics. In Meat-Eating and Human Evolution (eds Stanford, C. B. & Bunn, H. T.) 101–121 (Oxford University Press, 2001).
    Google Scholar 
    Werdelin, L. & Lewis, M. E. Plio-Pleistocene Carnivora of eastern Africa: species richness and turnover patterns. Zool. J. Linn. Soc. 144, 121–144. https://doi.org/10.1111/j.1096-3642.2005.00165.x (2005).Article 

    Google Scholar 
    Werdelin, L. & Lewis, M. E. Temporal change in functional richness and evenness in the eastern African Plio-Pleistocene carnivoran guild. PLoS ONE 8, e57944. https://doi.org/10.1371/journal.pone.0057944 (2013).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lewis, M. E. Carnivore guilds and the impact of hominin dispersals. In Human Dispersal and Species Movement: From Prehistory to the Present (eds Boivin, N. et al.) 29–61 (Cambridge University Press, 2017). https://doi.org/10.1017/9781316686942.003.Chapter 

    Google Scholar 
    Stiner, M. C. Competition theory and the case for Pleistocene hominin-carnivore co-evolution. J. Taphon. 10, 129–145 (2012).
    Google Scholar 
    Marean, C. W. Sabertooth cats and their relevance for early hominid diet and evolution. J. Hum. Evol. 18, 559–582 (1989).Article 

    Google Scholar 
    Martínez-Navarro, B. & Palmqvist, P. Presence of the African saber-toothed felid Megantereon whitei (Broom, 1937) (Mammalia, Carnivora, Machairodontinae) in Apollonia-1 (Mygdonia Basin, Macedonia, Greece). J. Archaeol. Sci. 23, 869–872. https://doi.org/10.1006/jasc.1996.0081 (1996).Article 

    Google Scholar 
    Arribas, A. & Palmqvist, P. On the ecological connection between sabre-tooths and hominids: Faunal dispersal events in the Lower Pleistocene and a review of the evidence for the first human arrival in Europe. J. Archaeol. Sci. 26, 571–585. https://doi.org/10.1006/jasc.1998.0346 (1999).Article 

    Google Scholar 
    Blumenschine, R. J. Characteristics of an early hominid scavenging niche. Curr. Anthropol. 28, 383–407. https://doi.org/10.1086/203544 (1987).Article 

    Google Scholar 
    Ewer, R. F. Sabre-toothed tigers. N. Biol. 17, 27–40 (1954).
    Google Scholar 
    Dominguez-Rodrigo, M. Flesh availability and bone modifications in carcasses consumed by lions: palaeoecological relevance in hominid foraging patterns. Palaeogeogr. Palaeoclimatol. Palaeoecol. 149, 373–388. https://doi.org/10.1016/S0031-0182(98)00213-2 (1999).Article 

    Google Scholar 
    Pobiner, B. L. & Blumenschine, R. J. A taphonomic perspective on Oldowan hominid encroachment on the carnivores paleoguild. J. Taphon. 1, 115–141 (2003).
    Google Scholar 
    Pobiner, B. L., Dumouchel, L. & Parkinson, J. A new semi-quantitative method for coding carnivore chewing damage with an application to modern African lion-damaged bones. Palaios 35, 302–315 (2020).ADS 
    Article 

    Google Scholar 
    Arribas, A. & Palmqvist, P. Taphonomy and palaeoecology of an assemblage of large mammals: hyaenid activity in the Lower Pleistocene site at Venta Micena (Orce, Guadix-Baza Basin, Granada, Spain). Geobios 31, 3–47. https://doi.org/10.1016/S0016-6995(98)80056-9 (1998).Article 

    Google Scholar 
    Palmqvist, P. et al. The giant hyena Pachycrocuta brevirostris: modelling the bone-cracking behavior of an extinct carnivore. Quat. Int. 243, 61–79. https://doi.org/10.1016/j.quaint.2010.12.035 (2011).Article 

    Google Scholar 
    Coca-Ortega, C. & Pérez-Claros, J. A. Characterizing ecomorphological patterns in hyenids: a multivariate approach using postcanine dentition. PeerJ 6, e6238. https://doi.org/10.7717/peerj.6238 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Pobiner, B. L. The zooarchaeology and paleoecology of early hominin scavenging. Evol. Anthropol. 29, 68–82. https://doi.org/10.1002/evan.21824 (2020).Article 
    PubMed 

    Google Scholar 
    Domínguez-Rodrigo, M., Pickering, T. R., Semaw, S. & Rogers, M. J. Cutmarked bones from Pliocene archaeological sites at Gona, Afar, Ethiopia: implications for the function of the world’s oldest stone tools. J. Hum. Evol. 48, 109–121. https://doi.org/10.1016/j.jhevol.2004.09.004 (2005).Article 
    PubMed 

    Google Scholar 
    Domínguez-Rodrigo, M. & Barba, R. The behavioral meaning of cut marks at the FLK Zinj level: the carnivore-hominid-carnivore hypothesis falsified (II). In Deconstructing Olduvai: A Taphonomic Study of the Bed I Sites (eds Domínguez-Rodrigo, M. et al.) 75–100 (Springer, 2007).Chapter 

    Google Scholar 
    Ferraro, J. V. et al. Earliest archaeological evidence of persistent hominin carnivory. PLoS ONE 8, e62174. https://doi.org/10.1371/journal.pone.0062174 (2013).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Oliver, J. S., Plummer, T. W., Hertel, F. & Bishop, L. C. Bovid mortality patterns from Kanjera South, Homa Peninsula, Kenya and FLK-Zinj, Olduvai Gorge, Tanzania: evidence for habitat mediated variability in Oldowan hominin hunting and scavenging behavior. J. Hum. Evol. 131, 61–75. https://doi.org/10.1016/j.jhevol.2019.03.009 (2019).Article 
    PubMed 

    Google Scholar 
    Bunn, H. T. Hunting, power scavenging, and butchering by Hadza foragers and by Plio-Pleistocene Homo. In Meat-Eating and Human Evolution (eds Stanford, C. B. & Bunn, H. T.) 199–218 (Oxford University Press, 2001).
    Google Scholar 
    Landeck, G. & García Garriga, J. New taphonomic data of the 1 Myr hominin butchery at Untermassfeld (Thuringia, Germany). Quat. Int. 436, 138–161. https://doi.org/10.1016/j.quaint.2016.11.016 (2017).Article 

    Google Scholar 
    Domínguez-Rodrigo, M. et al. On meat eating and human evolution: a taphonomic analysis of BK4b (Upper Bed II, Olduvai Gorge, Tanzania), and its bearing on hominin megafaunal consumption. Quat. Int. 322–323, 129–152. https://doi.org/10.1016/j.quaint.2013.08.015 (2014).Article 

    Google Scholar 
    Organista, E. et al. Taphonomic analysis of the level 3b fauna at BK, Olduvai Gorge. Quat. Int. 526, 116–128 (2019).Article 

    Google Scholar 
    Haynes, G. Prey bones and predators: potential ecologic information from analysis of bone sites. OSSA 7, 75–97 (1980).
    Google Scholar 
    Haynes, G. Evidence of carnivore gnawing on Pleistocene and recent mammalian bones. Paleobiology 6, 341–351. https://doi.org/10.1017/S0094837300006849 (1980).Article 

    Google Scholar 
    Haynes, G. A guide for differentiating mammalian carnivore taxa responsible for gnaw damage to herbivore limb bones. Paleobiology 9, 164–172 (1983).Article 

    Google Scholar 
    Sala, N., Arsuaga, J. L. & Haynes, G. Taphonomic comparison of bone modifications caused by wild and captive wolves (Canis lupus). Quat. Int. 330, 126–135. https://doi.org/10.1016/j.quaint.2013.08.017 (2014).Article 

    Google Scholar 
    Berta, A. The Plio-Pleistocene hyaena Chasmaporthetes ossifragus from Florida. J. Vertebr. Paleontol. 1, 341–356. https://doi.org/10.1080/02724634.1981.10011905 (1981).Article 

    Google Scholar 
    Anyonge, W. N. & Baker, A. Craniofacial morphology and feeding behavior in Canis dirus, the extinct Pleistocene dire wolf. J. Zool. 269, 309–316. https://doi.org/10.1111/j.1469-7998.2006.00043.x (2006).Article 

    Google Scholar 
    Figueirido, B., Pérez-Claros, J. A., Torregrosa, V., Martín-Serra, A. & Palmqvist, P. Demythologizing Arctodus simus, the ‘short-faced’ long-legged and predaceous bear that never was. J. Vertebr. Paleontol. 30, 262–275. https://doi.org/10.1080/02724630903416027 (2010).Article 

    Google Scholar 
    Pobiner, B. L. New actualistic data on the ecology and energetics of hominin scavenging opportunities. J. Hum. Evol. 80, 1–16 (2015).PubMed 
    Article 

    Google Scholar 
    Lautenschlager, S., Figueirido, B., Cashmore, D. D., Bendel, E.-M. & Stubbs, T. L. Morphological convergence obscures functional diversity in sabre-toothed carnivores. Proc. R. Soc. B. 287, 20201818. https://doi.org/10.1098/rspb.2020.1818 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Figueirido, B., Lautenschlager, S., Pérez-Ramos, A. & Van Valkenburgh, B. Distinct predatory behaviors in scimitar- and dirk-toothed sabertooth cats. Curr. Biol. 28, 3260-3266.e3. https://doi.org/10.1016/j.cub.2018.08.012 (2018).CAS 
    Article 
    PubMed 

    Google Scholar 
    Hartstone-Rose, A. Reconstructing the diets of extinct South African carnivorans from premolar ‘intercuspid notch’ morphology. J. Zool. 285, 119–127. https://doi.org/10.1111/j.1469-7998.2011.00821.x (2011).Article 

    Google Scholar 
    Van Valkenburgh, B. Costs of carnivory: tooth fracture in Pleistocene and recent carnivorans. Biol. J. Lin. Soc. 96, 68–81. https://doi.org/10.1111/j.1095-8312.2008.01108.x (2009).Article 

    Google Scholar 
    Thieme, H. Lower Palaeolithic hunting spears from Germany. Nature 385, 807–810. https://doi.org/10.1038/385807a0 (1997).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Conard, N. J., Serangeli, J., Gerlinde, B. & Veerle, R. A 300,000-year-old throwing stick from Schöningen, northern Germany, documents the evolution of human hunting. Nat. Ecol. Evol. 4, 690–693 (2020).PubMed 
    Article 

    Google Scholar 
    Austin, L. A., Bergman, C. A., Roberts, M. B. & Wilhelmsen, K. H. Archaeology of the excavated areas. In Boxgrove: A Middle Pleistocene Hominid Site at Eartham Quarry (eds Roberts, M. B. & Parfitt, S. A.) 312–378 (Boxgrove, 1999).
    Google Scholar 
    Domínguez-Rodrigo, M., Baquedano, E., Organista, E. et al. Early Pleistocene faunivorous hominins were not kleptoparasitic, and this impacted the evolution of human anatomy and socio-ecology. Sci Rep 11, 16135 (2021). https://doi.org/10.1038/s41598-021-94783-4ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gohn, G. S. Late Mesozoic and early Cenozoic geology of the Atlantic Coastal Plain: North Carolina to Florida. In The Geology of North America, Volume I-2, The Atlantic Continental Margin (eds Sheridan, R. E. & Grow, J. A.) 107–130 (Geological Society of America, Boulder, CO, 1988).
    Google Scholar 
    Pirkle, E. C. Notes on physiographic features of Alachua County, Florida. Q. J. Fla. Acad. Sci. 19, 168–182 (1956).
    Google Scholar 
    Beck, B. F. A generalized genetic framework for the development of sinkholes and karst in Florida, U.S.A. Environ. Geol. Water Sci. 8, 5–18. https://doi.org/10.1007/BF02525554 (1986).ADS 
    Article 

    Google Scholar 
    Beck, B. F. & Sinclair, W. C. Sinkholes in Florida: An Introduction (The Florida Sinkhole Research Institute, 1986).
    Google Scholar 
    Brinkman, R. Florida Sinkholes: Science and Policy (University of Florida Press, 2013).Book 

    Google Scholar 
    Hines, A. C. Geologic History of Florida: Major Events that Formed the Sunshine State (University of Florida Press, 2013).
    Google Scholar 
    Bader, R. S. Two Pleistocene mammalian faunas from Alachua County, Florida. Bull. Fla State Mus. 2, 53–75 (1957).
    Google Scholar 
    Patton, T. H. An Oligocene land vertebrate fauna from Florida. J. Paleontol. 43, 543–546 (1969).
    Google Scholar 
    Pratt, A. E. Taphonomy of the large vertebrate fauna from the Thomas Farm Locality (Miocene, Hemingfordian), Gilchrist County, Florida, Bulletin of the Florida Museum of. Nat. Hist. 35, 35–130 (1990).
    Google Scholar 
    Ruez, D. R. Jr. Mammalian taphonomy of the Early Irvingtonian (Late Pliocene) Inglis 1C fauna (Citrus County, Florida). Southeast. Geol. 41, 159–168 (2002).
    Google Scholar 
    Hansen, B. C. S., Grimm, E. C. & Watts, W. A. Palynology of the Peace Creek site, Polk County, Florida. Geol. Soc. Am. Bull. 113, 682–692 (2001).ADS 
    Article 

    Google Scholar 
    Morgan, G. S. & Emslie, S. D. Tropical and western influences in vertebrate faunas from the Pliocene and Pleistocene of Florida. Quat. Int. 217, 143–158. https://doi.org/10.1016/j.quaint.2009.11.030 (2010).Article 

    Google Scholar 
    Yann, L. T. & DeSantis, L. R. G. Effects of Pleistocene climates on local environments and dietary behavior of mammals in Florida. Palaeogeogr. Palaeoclimatol. Palaeoecol. 414, 370–381. https://doi.org/10.1016/j.palaeo.2014.09.020 (2014).Article 

    Google Scholar 
    Perrotti, A. G., Winsborough, B., Halligan, J. J. & Waters, M. R. Reconstructing terminal Pleistocene-early Holocene environmental change at Page-Ladson, Florida using diatom evidence. PaleoAmerica 6, 181–193. https://doi.org/10.1080/20555563.2019.1689010 (2020).Article 

    Google Scholar 
    Tanner, B. R., Work, K. A. & Evans, J. M. The potential of organic sediments in Florida spring runs as records of environmental change. Southeast. Geogr. 60, 200–214. https://doi.org/10.1353/sgo.2020.0017 (2020).Article 

    Google Scholar 
    Simpson, G. G. The Extinct Land Mammals of Florida (Florida Geological Survey, 1928).
    Google Scholar 
    Simpson, G. G. Tertiary land mammals of Florida. Bull. Am. Mus. Nat. Hist. 59, 149–211 (1930).
    Google Scholar 
    Olsen, S. J. Fossil Mammals of Florida (Florida Geological Survey, 1959).
    Google Scholar 
    Webb, S. D. Pleistocene Mammals of Florida (University of Florida Press, 1974).
    Google Scholar 
    Tihen, J. A. Rana grylio from the Pleistocene of Florida. Herpetologica 8, 107 (1952).
    Google Scholar 
    Brodkorb, P. Pleistocene birds from Haile, Florida. Wilson Bull. 65, 49–50 (1953).
    Google Scholar 
    Brodkorb, P. Another new rail from the Pleistocene of Florida. The Condor. 56, 103–104 (1954).
    Google Scholar 
    Brodkorb, P. Fossil birds from the Alachua clay of Florida, Florida Geological Survey, Contributions to Florida Vertebrate Paleontology. Spec. Publ. 2, 1–17 (1963).
    Google Scholar 
    Auffenburg, W. Additional specimens of Gavialosuchus americanus (Sellards) from a new locality in Florida. Q. J. Fla. Acad. Sci. 17, 185–209 (1954).
    Google Scholar 
    Auffenburg, W. Glass lizards (Ophisaurus) in the Pleistocene and Pliocene of Florida. Herpetologica 11, 133–136 (1955).
    Google Scholar 
    Auffenburg, W. Additional records of Pleistocene lizards from Florida. Q. J. Fla. Acad. Sci. 19, 157–167 (1956).
    Google Scholar 
    Auffenburg, W. A new species of Bufo from the Pliocene of Florida. Q. J. Fla. Acad. Sci. 20, 14–20 (1957).
    Google Scholar 
    Goin, C. J. & Auffenburg, W. The fossil salamanders of the Family Sirenidae, Bulletin of the Museum of Comparative. Zoology 113, 497–514 (1955).
    Google Scholar 
    Ligon, J. D. A Pleistocene avifauna from Haile, Florida. Bull. Fla. State Mus. 10, 127–158 (1965).
    Google Scholar 
    Kinsey, P. E. A new species of Mylohyus peccary from the Florida early Pleistocene. In Pleistocene Mammals of Florida (ed. Webb, S. D.) 158–169 (University of Florida Press, 1974).
    Google Scholar 
    Martin, R. A. Fossil vertebrates from the Haile XIVA fauna, Alachua County. In Pleistocene Mammals of Florida (ed. Webb, S. D.) 100–113 (University of Florida Press, 1974).
    Google Scholar 
    Robertson, J. S. Fossil Bison of Florida. In Pleistocene Mammals of Florida (ed. Webb, S. D.) 214–246 (University of Florida Press, 1974).
    Google Scholar 
    Robertson, J. S. Late Pliocene mammals from Haile XV A, Alachua County, Florida. Bull. Fla. State Mus. 20, 111–186 (1976).ADS 

    Google Scholar 
    Webb, S. D. Pleistocene llamas of Florida, with a brief review of the Lamini. In Pleistocene Mammals of Florida (ed. Webb, S. D.) 170–213 (University of Florida Press, 1974).
    Google Scholar 
    Campbell, K. E. An early Pleistocene avifauna from Haile XVA, Florida. Wilson Bull. 88, 345–347 (1976).
    Google Scholar 
    Morgan, G. S., Linares, O. J. & Ray, C. E. New species of fossil vampire bats (Mammalia, Chiroptera, Desmodontidae) from Florida and Venezuela. Proc. Biol. Soc. Wash. 101, 912–928 (1988).
    Google Scholar 
    Hulbert, R. C. A new late Pliocene porcupine (Rodentia: Erethizontidae) from Florida. J. Vertebr. Paleontol. 17, 623–626. https://doi.org/10.1080/02724634.1997.10011010 (1997).Article 

    Google Scholar 
    de Iuliis, G. & Cartelle, C. A new giant megatheriine ground sloth (Mammalia: Xenarthra: Megatheriidae) from the late Blancan to early Irvingtonian of Florida. Zool. J. Linn. Soc. 127, 495–515 (1999).Article 

    Google Scholar 
    Portell, R. W. & Hulbert, R. C. Haile Quarries Fieldguide Newberry (Southeastern Geological Society, 2011).
    Google Scholar 
    Morgan, G. S. Neotropical Chiroptera from the Pliocene and Pleistocene of Florida. Bull. Am. Mus. Nat. Hist. 206, 176–213 (1991).
    Google Scholar 
    Hulbert, R. C., Morgan, G. S. & Webb, S. D. Paleontology and geology of the Leisey shell pits, early Pleistocene of Florida. Bull. Fla. Mus. Nat. Hist. 37, 1–660 (1995).
    Google Scholar 
    Berta, A. Fossil carnivores from the Leisey Shell Pits, Hillsborough County, Florida. Bull. Am. Mus. Nat. Hist. 37, 463–499 (1995).
    Google Scholar 
    Hulbert, R. C. The giant tapir, Tapirus haysii, from Leisey Shell Pit 1A and other Florida Invingtonian localities. Bull. Am. Mus. Nat. Hist. 37, 515–551 (1995).
    Google Scholar 
    Wright, D. B. Tayassuidae of the Irvingtonian Leisey Shell Pit local fauna, Hillsborough County, Florida. Bull. Am. Mus. Nat. Hist. 37, 603–619 (1995).
    Google Scholar 
    Martin, L. D., Babiarz, J. P. & Naples, V. L. The osteology of a cookie-cutter cat, Xenosmilus hodsonae. In The Other Saber-Tooths: Scimitar-Tooth Cats of the Western Hemisphere (eds Naples, V. L. et al.) 43–97 (Johns Hopkins University Press, 2011).
    Google Scholar 
    Gifford-Gonzalez, D. Bones are not enough: analogues, knowledge, and interpretive strategies in zooarchaeology. J. Anthropol. Archaeol. 10, 215–254. https://doi.org/10.1016/0278-4165(91)90014-O (1991).Article 

    Google Scholar 
    Capaldo, S. D. Experimental determinations of carcass processing by Plio-Pleistocene hominids and carnivores at FLK 22 (Zinjanthropus), Olduvai Gorge, Tanzania. J. Hum. Evol. 33, 555–597. https://doi.org/10.1006/jhev.1997.0150 (1997).CAS 
    Article 
    PubMed 

    Google Scholar 
    Johnson, E. Current developments in bone technology. Adv. Archeol. Method Theory 8, 157–235. https://doi.org/10.1016/B978-0-12-003108-5.50010-5 (1985).Article 

    Google Scholar 
    Binford, L. R. Bones: Ancient Men and Modern Myths (Academic Press, 1981).
    Google Scholar 
    Dominguez-Rodrigo, M. & Barba, R. New estimates of tooth-mark and percussion-mark frequencies at the FLK Zinjanthropus level: the carnivore–hominid–carnivore hypothesis falsified (I). In Deconstructing Olduvai: A Taphonomic Study of the Bed I Sites (eds Dominguez-Rodrigo, M. et al.) 39–74 (Springer, 2007).Chapter 

    Google Scholar 
    Domínguez-Rodrigo, M. et al. A new methodological approach to the taphonomic study of paleontological and archaeological faunal assemblages: a preliminary case study from Olduvai Gorge (Tanzania). J. Archaeol. Sci. 59, 35–53. https://doi.org/10.1016/j.jas.2015.04.007 (2015).Article 

    Google Scholar 
    Andrés, M., Gidna, A. O., Yravedra, J. & Domínguez-Rodrigo, M. A study of dimensional differences of tooth marks (pits and scores) on bones modified by small and large carnivores. Archaeol. Anthropol. Sci. 4, 209–219. https://doi.org/10.1007/s12520-012-0093-4 (2012).Article 

    Google Scholar 
    Behrensmeyer, A. K. Taphonomic and ecologic information from bone weathering. Paleobiology 4, 150–162. https://doi.org/10.1017/S0094837300005820 (1978).Article 

    Google Scholar 
    Behrensmeyer, A. K., Gordon, K. D. & Yanagi, G. T. Trampling as a cause of bone surface damage and pseudo-cutmarks. Nature 319, 768–771 (1986).ADS 
    Article 

    Google Scholar 
    Egeland, C. P. et al. The taphonomy of fallow deer (Dama dama) skeletons from Denmark and its bearing on the pre-Weichselian occupation of northern Europe by humans. Archaeol. Anthropol. Sci. 6, 31–61 (2014).Article 

    Google Scholar 
    H.T. Bunn, Meat-Eating and Human Evolution: Studies on the Diet and Subsistence Patterns of Plio-Pleistocene Hominids in East Africa, Ph.D. Dissertation, University of California, 1982. More

  • in

    Urban-adapted mammal species have more known pathogens

    Morse, S. S. et al. Prediction and prevention of the next pandemic zoonosis. Lancet 380, 1956–1965 (2012).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Jones, K. E. et al. Global trends in emerging infectious diseases. Nature 451, 990–993 (2008).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Keesing, F. et al. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468, 647–652 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Carlson, C. J. et al. Climate change will drive novel cross-species viral transmission. Preprint at bioRxiv https://doi.org/10.1101/2020.01.24.918755 (2020).Gibb, R. et al. Zoonotic host diversity increases in human-dominated ecosystems. Nature https://doi.org/10.1038/s41586-020-2562-8 (2020).Loh, E. H. et al. Targeting transmission pathways for emerging zoonotic disease surveillance and control. Vector Borne Zoonotic Dis. 15, 432–437 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hassell, J. M., Begon, M., Ward, M. J. & Fèvre, E. M. Urbanization and disease emergence: dynamics at the wildlife–livestock–human interface. Trends Ecol. Evol. 32, 55–67 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Cohen, J. M., Sauer, E. L., Santiago, O., Spencer, S. & Rohr, J. R. Divergent impacts of warming weather on wildlife disease risk across climates. Science 370, eabb1702 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Murray, M. H. et al. City sicker? A meta-analysis of wildlife health and urbanization. Front. Ecol. Environ. 17, 575–583 (2019).Article 

    Google Scholar 
    Becker, D. J., Hall, R. J., Forbes, K. M., Plowright, R. K. & Altizer, S. Anthropogenic resource subsidies and host–parasite dynamics in wildlife. Phil. Trans. R. Soc. B 373, 20170086 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Werner, C. S. & Nunn, C. L. Effect of urban habitat use on parasitism in mammals: a meta-analysis. Proc. Biol. Sci. 287, 20200397 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    Becker, D. J., Streicker, D. G. & Altizer, S. Linking anthropogenic resources to wildlife–pathogen dynamics: a review and meta-analysis. Ecol. Lett. 18, 483–495 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Becker, D. J. et al. Macroimmunology: the drivers and consequences of spatial patterns in wildlife immune defense. J. Anim. Ecol. 89, 972–995 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Albery, G. F. & Becker, D. J. Fast-lived hosts and zoonotic risk. Trends Parasitol. https://doi.org/10.1016/j.pt.2020.10.012 (2021).Seto, K. C., Güneralp, B. & Hutyra, L. R. Global forecasts of urban expansion to 2030 and direct impacts on biodiversity and carbon pools. Proc. Natl Acad. Sci. USA 109, 16083–16088 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Chen, G. et al. Global projections of future urban land expansion under shared socioeconomic pathways. Nat. Commun. 11, 537 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Gao, J. & O’Neill, B. C. Mapping global urban land for the twenty-first century with data-driven simulations and shared socioeconomic pathways. Nat. Commun. 11, 2302 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Santini, L. et al. One strategy does not fit all: determinants of urban adaptation in mammals. Ecol. Lett. 22, 365–376 (2019).PubMed 
    Article 

    Google Scholar 
    Ostfeld, R. S. et al. Life history and demographic drivers of reservoir competence for three tick-borne zoonotic pathogens. PLoS ONE 9, e107387 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Olival, K. J. et al. Host and viral traits predict zoonotic spillover from mammals. Nature 546, 646–650 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Mollentze, N. & Streicker, D. G. Viral zoonotic risk is homogenous among taxonomic orders of mammalian and avian reservoir hosts. Proc. Natl Acad. Sci. USA 117, 9423–9430 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Gutiérrez, J. S., Piersma, T. & Thieltges, D. W. Micro- and macroparasite species richness in birds: the role of host life history and ecology. J. Anim. Ecol. 88, 1226–1239 (2019).PubMed 
    Article 

    Google Scholar 
    Teitelbaum, C. S. et al. A comparison of diversity estimators applied to a database of host–parasite associations. Ecography 43, 1316–1328 (2019).Article 

    Google Scholar 
    Jorge, F. & Poulin, R. Poor geographical match between the distributions of host diversity and parasite discovery effort. Proc. R. Soc. B 285, 20180072 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Allen, T. et al. Global hotspots and correlates of emerging zoonotic diseases. Nat. Commun. 8, 1124 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Gibb, R. et al. Mammal virus diversity estimates are unstable due to accelerating discovery effort. Biol. Lett. https://doi.org/10.1098/rsbl.2021.0427 (2022).Hughes, A. et al. Sampling biases shape our view of the natural world. Ecography 44, 1259–1269 (2021).Article 

    Google Scholar 
    Estes, L. et al. The spatial and temporal domains of modern ecology. Nat. Ecol. Evol. 2, 819–826 (2018).PubMed 
    Article 

    Google Scholar 
    Titley, M. A., Snaddon, J. L. & Turner, E. C. Scientific research on animal biodiversity is systematically biased towards vertebrates and temperate regions. PLoS ONE 12, e0189577 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Lloyd-Smith, J. O. et al. Should we expect population thresholds for wildlife disease? Trends Ecol. Evol. 20, 511–519 (2005).PubMed 
    Article 

    Google Scholar 
    Cummings, C. R. et al. Foraging in urban environments increases bactericidal capacity in plasma and decreases corticosterone concentrations in white ibises. Front. Ecol. Evol. 8, 575980 (2020).Article 

    Google Scholar 
    Hwang, J. et al. Anthropogenic food provisioning and immune phenotype: association among supplemental food, body condition, and immunological parameters in urban environments. Ecol. Evol. 8, 3037–3046 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Strandin, T., Babayan, S. A. & Forbes, K. M. Reviewing the effects of food provisioning on wildlife immunity. Phil. Trans. R. Soc. B 373, 20170088 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Downs, C. J., Dochtermann, N. A., Ball, R., Klasing, K. C. & Martin, L. B. The effects of body mass on immune cell concentrations of mammals. Am. Nat. 195, 107–114 (2020).PubMed 
    Article 

    Google Scholar 
    Downs, C. J. et al. Extreme hyperallometry of mammalian antibacterial defenses. Preprint at bioRxiv https://doi.org/10.1101/2020.09.04.242107 (2020).Becker, D. J., Seifert, S. N. & Carlson, C. J. Beyond infection: integrating competence into reservoir host prediction. Trends Ecol. Evol. 35, 1062–1065 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hanson, D. A., Britten, H. B., Restani, M. & Washburn, L. R. High prevalence of Yersinia pestis in black-tailed prairie dog colonies during an apparent enzootic phase of sylvatic plague. Conserv. Genet. 8, 789–795 (2007).CAS 
    Article 

    Google Scholar 
    Gecchele, L. V., Pedersen, A. B. & Bell, M. Fine-scale variation within urban landscapes affects marking patterns and gastrointestinal parasite diversity in red foxes. Ecol. Evol. 10, 13796–13809 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Albery, G. F., Sweeny, A. R., Becker, D. J. & Bansal, S. Fine-scale spatial patterns of wildlife disease are common and understudied. Funct. Ecol. https://doi.org/10.1111/1365-2435.13942 (2021).Jones, K. E. et al. PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals. Ecology 90, 2648–2648 (2009).Article 

    Google Scholar 
    Fritz, S. A., Bininda-Emonds, O. R. P. & Purvis, A. Geographical variation in predictors of mammalian extinction risk: big is bad, but only in the tropics. Ecol. Lett. 12, 538–549 (2009).PubMed 
    Article 

    Google Scholar 
    Albery, G. F., Eskew, E. A., Ross, N. & Olival, K. J. Predicting the global mammalian viral sharing network using phylogeography. Nat. Commun. https://doi.org/10.1038/s41467-020-16153-4 (2020).IUCN Red List of Threatened Species Version 2019-2 (IUCN, 2019); https://www.iucnredlist.orgBecker, D. J. et al. Optimising predictive models to prioritise viral discovery in zoonotic reservoirs. Lancet Microbe https://doi.org/10.1016/S2666-5247(21)00245-7 (2022).Mason, P. Parasites of deer in New Zealand. N. Zeal. J. Zool. 21, 39–47 (1994).Article 

    Google Scholar 
    Wilman, H. et al. EltonTraits 1.0: species-level foraging attributes of the world’s birds and mammals. Ecology 95, 2027 (2014).Article 

    Google Scholar 
    Plourde, B. T. et al. Are disease reservoirs special? Taxonomic and life history characteristics. PLoS ONE 12, e0180716 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Gibb, R. et al. Data proliferation, reconciliation, and synthesis in viral ecology. Bioscience https://doi.org/10.1101/2021.01.14.426572 (2021).Stephens, P. R. et al. Global mammal parasite database version 2.0. Ecology 98, 1476 (2017).PubMed 
    Article 

    Google Scholar 
    Wardeh, M., Risley, C., Mcintyre, M. K., Setzkorn, C. & Baylis, M. Database of host–pathogen and related species interactions, and their global distribution. Sci. Data 2, 150049 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Shaw, L. P. et al. The phylogenetic range of bacterial and viral pathogens of vertebrates. Mol. Ecol. 29, 3361–3379 (2020).PubMed 
    Article 

    Google Scholar 
    Chamberlain, S. A. & Szöcs, E. taxize: taxonomic search and retrieval in R. F1000Res https://doi.org/10.12688/f1000research.2-191.v2 (2013).Carlson, C. J. et al. The Global Virome in One Network (VIRION): an atlas of vertebrate–virus associations. mBio 13, e0298521 (2022).Article 

    Google Scholar 
    Lindgren, F. & Rue, H. Bayesian spatial modelling with R-INLA. J. Stat. Softw. 63, 1–25 (2015).Article 

    Google Scholar 
    Lindgren, F., Rue, H. & Lindstrom, J. An explicit link between Gaussian fields and Gaussian Markov random fields: the stochastic partial differential equation approach. J. R. Stat. Soc. B 73, 423–498 (2011).Article 

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

    Google Scholar 
    Winter, D. J. rentrez: an R package for the NCBI eUtils API. R J. 9, 520–526 (2017).Article 

    Google Scholar 
    Shipley, B. Confirmatory path analysis in a generalized multilevel context. Ecology 90, 363–368 (2009).PubMed 
    Article 

    Google Scholar 
    Carlson, C. J., Dallas, T. A., Alexander, L. W., Phelan, A. L. & Phillips, A. J. What would it take to describe the global diversity of parasites? Proc. R. Soc. B 287, 20201841 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

  • in

    Portfolio effects and functional redundancy contribute to the maintenance of octocoral forests on Caribbean reefs

    Loya, Y. et al. Coral bleaching: the winners and the losers. Ecol. Lett. 4, 122–131. https://doi.org/10.1046/j.1461-0248.2001.00203.x (2001).Article 

    Google Scholar 
    Hughes, T. P. et al. Global warming transforms coral reef assemblages. Nature 556, 492–496 (2018).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Darling, E. S., Alvarez-Filip, L., Oliver, T. A., McClanahan, T. R. & Côté, I. M. Evaluating life-history strategies of reef corals from species traits. Ecol. Lett. 15, 1378–1386 (2012).PubMed 
    Article 

    Google Scholar 
    Toth, L. T. et al. The unprecedented loss of Florida’s reef-building corals and the emergence of a novel coral-reef assemblage. Ecology 100, e02781. https://doi.org/10.1002/ecy.2781 (2019).CAS 
    Article 
    PubMed 

    Google Scholar 
    Green, D. H., Edmunds, P. J. & Carpenter, R. C. Increasing relative abundance of Porites astreoides on Caribbean reefs mediated by an overall decline in coral cover. Mar. Ecol. Prog. Ser. 359, 1–10 (2008).ADS 
    Article 

    Google Scholar 
    Alvarez-Filip, L., Carricart-Ganivet, J. P., Horta-Puga, G. & Iglesias-Prieto, R. Shifts in coral-assemblage composition do not ensure persistence of reef functionality. Sci. Rep. 3, 3486. https://doi.org/10.1038/srep03486 (2013).ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Hughes, T. P. et al. Global warming and recurrent mass bleaching of corals. Nature 543, 373–377 (2017).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Hughes, T. P. et al. Ecological memory modifies the cumulative impact of recurrent climate extremes. Nat. Clim. Change 9, 40–43 (2019).ADS 
    Article 

    Google Scholar 
    Hoegh-Guldberg, O., Poloczanska, E. S., Skirving, W. & Dove, S. Coral reef ecosystems under climate change and ocean acidification. Front. Mar. Sci. https://doi.org/10.3389/fmars.2017.00158 (2017).Article 

    Google Scholar 
    Gardner, T. A., Côté, I. M., Gill, J. A., Grant, A. & Watkinson, A. R. Long-term region-wide declines in Caribbean corals. Science 301, 958–960 (2003).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Jackson, J., Donovan, M., Cramer, K. & Lam, V. Status and trends of Caribbean coral reefs. Global Coral Reef Monitoring Network, IUCN, Gland, Switzerland, 1970–2012 (2014).Bruno, J. F., Sweatman, H., Precht, W. F., Selig, E. R. & Schutte, V. G. Ecosystem-based management. Ecology 90, 1478–1484 (2009).PubMed 
    Article 

    Google Scholar 
    Roff, G. & Mumby, P. J. Global disparity in the resilience of coral reefs. Trends Ecol. Evol. 27, 404–413 (2012).PubMed 
    Article 

    Google Scholar 
    Bak, R. P. M., Lambrechts, D. Y. M., Joenje, M., Nieuwland, G. & Van Veghel, M. L. J. Long-term changes on coral reefs in booming populations of a competitive colonial ascidian. Mar. Ecol. Prog. Ser. 133, 303–306 (1996).ADS 
    Article 

    Google Scholar 
    Norström, A. V., Nyström, M., Lokrantz, J. & Folke, C. Alternative states on coral reefs: beyond coral–macroalgal phase shifts. Mar. Ecol. Prog. Ser. 376, 295–306 (2009).ADS 
    Article 

    Google Scholar 
    Lenz, E. A., Bramanti, L., Lasker, H. R. & Edmunds, P. J. Long-term variation of octocoral populations in St. John, US Virgin Islands. Coral Reefs 34, 1099–1109 (2015).ADS 
    Article 

    Google Scholar 
    Pawlik, J. R. & McMurray, S. E. The emerging ecological and biogeochemical importance of sponges on coral reefs. Ann. Rev. Mar Sci. 12, 315–337 (2020).PubMed 
    Article 

    Google Scholar 
    Lasker, H. R., Bramanti, L., Tsounis, G. & Edmunds, P. J. in Advances in Marine Biology Vol. 87 (ed. Riegl, B. M.) 361–410 (Academic Press, 2020).
    Google Scholar 
    Pearson, R. Recovery and recolonization of coral reefs. Mar. Ecol. Prog. Ser. 4, 105–122 (1981).ADS 
    Article 

    Google Scholar 
    Connell, J. H., Hughes, T. P. & Wallace, C. C. A 30-year study of coral abundance, recruitment, and disturbance at several scales in space and time. Ecol. Monogr. 67, 461–488 (1997).Article 

    Google Scholar 
    França, F. M. et al. Climatic and local stressor interactions threaten tropical forests and coral reefs. Philos. Trans. R. Soc. B 375, 20190116 (2020).Article 

    Google Scholar 
    Ruzicka, R. et al. Temporal changes in benthic assemblages on Florida Keys reefs 11 years after the 1997/1998 El Niño. Mar. Ecol. Prog. Ser. 489, 125–141 (2013).ADS 
    Article 

    Google Scholar 
    Sánchez, J. A. et al. in Mesophotic Coral Ecosystems (eds Loya, Y. et al.) 729–747 (Springer International Publishing, 2019).Chapter 

    Google Scholar 
    Tsounis, G., Edmunds, P. J., Bramanti, L., Gambrel, B. & Lasker, H. R. Variability of size structure and species composition in Caribbean octocoral communities under contrasting environmental conditions. Mar. Biol. 165, 29. https://doi.org/10.1007/s00227-018-3286-2 (2018).Article 

    Google Scholar 
    Kinzie, R. A. III. The zonation of West Indian gorgonians. Bull. Mar. Sci. 23, 93–155 (1973).
    Google Scholar 
    Yoshioka, P. M. & Yoshioka, B. B. A comparison of the survivorship and growth of shallow-water gorgonian species of Puerto Rico. Mar. Ecol. Prog. Ser. 69, 253–260 (1991).ADS 
    Article 

    Google Scholar 
    De’ath, G., Fabricius, K. E., Sweatman, H. & Puotinen, M. The 27–year decline of coral cover on the Great Barrier Reef and its causes. Proc. Natl. Acad. Sci. USA 109, 17995–17999 (2012).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Newman, M. J., Paredes, G. A., Sala, E. & Jackson, J. B. Structure of Caribbean coral reef communities across a large gradient of fish biomass. Ecol. Lett. 9, 1216–1227 (2006).PubMed 
    Article 

    Google Scholar 
    Tilman, D. The ecological consequences of changes in biodiversity: a search for general principles. Ecology 80, 1455–1474 (1999).
    Google Scholar 
    Lawton, J. H. & Brown, V. K. in Biodiversity and Ecosystem Function (eds Schulze, E. D. & Mooney, H. A.) 255–270 (Springer, 1994).Chapter 

    Google Scholar 
    Loreau, M. et al. Biodiversity as insurance: from concept to measurement and application. Biol. Rev. 96(5), 2333–2354 (2021).PubMed 
    Article 

    Google Scholar 
    Bellwood, D. R., Stret, R. P., Brandl, S. J. & Tebbett, S. B. The meaning of the term ‘function’ in ecology: a coral reef perspective. Funct. Ecol. 33, 948–961 (2018).Article 

    Google Scholar 
    Caswell, H. Construction, analysis, and interpretation. Sunderland: Sinauer 585, 258–277 (2001).
    Google Scholar 
    Bayer, F. M. The shallow-water Octocorallia of the West Indian region. Stud. Fauna Curacao Caribb. Isl. 12, 1–373 (1961).
    Google Scholar 
    Rossi, S., Bramanti, L., Gori, A. & Orejas, C. An overview of the animal forests of the world. In Marine Animal Forest (ed. Rossi, S.) 1–25 (Springer, 2017).Chapter 

    Google Scholar 
    Sánchez, J. A. Diversity and evolution of octocoral animal forests at both sides of tropical america. in Marine Animal Forests (eds Rossi, S. et al.) (Springer, 2016).
    Google Scholar 
    Thibaut, L. M. & Connolly, S. R. Understanding diversity–stability relationships: towards a unified model of portfolio effects. Ecol. Lett. 16, 140–150 (2013).PubMed 
    Article 

    Google Scholar 
    Schindler, D. E., Armstrong, J. B. & Reed, T. E. The portfolio concept in ecology and evolution. Front. Ecol. Environ. 13, 257–263 (2015).Article 

    Google Scholar 
    Biggs, C. R. et al. Does functional redundancy affect ecological stability and resilience? A review and meta-analysis. Ecosphere 11, e03184 (2020).Article 

    Google Scholar 
    Anderson, S. C., Moore, J. W., McClure, M. M., Dulvy, N. K. & Cooper, A. B. Portfolio conservation of metapopulations under climate change. Ecol. Appl. 25, 559–572 (2015).PubMed 
    Article 

    Google Scholar 
    Mellin, C., MacNeil, A. M., Cheal, A. J., Emslie, M. J. & Caley, J. M. Marine protected areas increase resilience among coral reef communities. Ecol. Lett. 19, 629–637 (2016).PubMed 
    Article 

    Google Scholar 
    Webster, N. et al. Host-associated coral reef microbes respond to the cumulative pressures of ocean warming and ocean acidification. Sci. rep. 6, 1–9 (2016).Article 
    CAS 

    Google Scholar 
    Tsounis, G. & Edmunds, P. J. Three decades of coral reef community dynamics in St. John, USVI: a contrast of scleractinians and octocorals. Ecosphere 8, e01646 (2017).Article 

    Google Scholar 
    Hurlbert, S. H. Pseudoreplication and the design of ecological field experiments. Ecol. Monogr. 54, 187–211 (1984).Article 

    Google Scholar 
    Tsounis, G., Edmunds, P. J., Bramanti, L., Gambrel, B. & Lasker, H. R. Variability of size structure and species composition in Caribbean octocoral communities under contrasting environmental conditions. Mar. Biol. 165, 1–14 (2018).Article 

    Google Scholar 
    Browning, T. N. et al. Widespread deposition in a coastal bay following three major 2017 hurricanes (Irma, Jose, and Maria). Sci. Rep. 9, 1–13 (2019).CAS 
    Article 

    Google Scholar 
    Edmunds, P. J. Three decades of degradation lead to diminished impacts of severe hurricanes on Caribbean reefs. Ecology 100, e02587 (2019).PubMed 
    Article 

    Google Scholar 
    Clarke, K. & Warwick, R. Quantifying structural redundancy in ecological communities. Oecologia 113, 278–289 (1998).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Menge, B. A., Berlow, E. L., Blanchette, C. A., Navarrete, S. A. & Yamada, S. B. The keystone species concept: variation in interaction strength in a rocky intertidal habitat. Ecol. Monogr. 64, 249–286 (1994).Article 

    Google Scholar 
    Frost, T. M., Carpenter, S. R., Ives, A. R. & Kratz, T. K. in Linking Species & Ecosystems (eds Jones, C. G. & Lawton, J. H.) 224–239 (Springer, 1995).Chapter 

    Google Scholar 
    Lasker, H., Martínez-Quintana, Á., Bramanti, L. & Edmunds, P. J. Resilience of octocoral forests to catastrophic storms. Sci. Rep. 10, 1–8 (2020).Article 
    CAS 

    Google Scholar 
    Goffredo, S. & Lasker, H. R. Modular growth of a gorgonian coral can generate predictable patterns of colony growth. J. Exp. Mar. Biol. Ecol. 336, 221–229 (2006).Article 

    Google Scholar 
    Grigg, R. W. Growth rings: annual periodicity in two gorgonian corals. Ecology 55, 876–881 (1974).Article 

    Google Scholar 
    Grigg, R. W. Resource management of precious corals a review and application ton shallow water reef building corals. Mar. Ecol. 5, 57–74 (1984).ADS 
    Article 

    Google Scholar 
    Clarke, K. R. & Gorley, R. N. Primer v6: User Manual/Tutorial (PRIMER-E Ltd., 2006).
    Google Scholar 
    Schutte, V. G., Selig, E. R. & Bruno, J. F. Regional spatio-temporal trends in Caribbean coral reef benthic communities. Mar. Ecol. Prog. Ser. 402, 115–122 (2010).ADS 
    Article 

    Google Scholar 
    Edmunds, P. J. Decadal-scale changes in the community structure of coral reefs of St. John, US Virgin Islands. Mar. Ecol. Prog. Ser. 489, 107–123 (2013).ADS 
    Article 

    Google Scholar 
    Chollett, I., Mumby, P. J., Müller-Karger, F. E. & Hu, C. Physical environments of the Caribbean Sea. Limnol. Oceanogr. 57, 1233–1244 (2012).ADS 
    Article 

    Google Scholar 
    Fowell, S. E. et al. Historical trends in pH and carbonate biogeochemistry on the Belize Mesoamerican Barrier Reef System. Geophys. Res. Lett. 45, 3228–3237. https://doi.org/10.1002/2017GL076496 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    Edmunds, P. J. & Lasker, H. R. Regulation of population size of arborescent octocorals on shallow Caribbean reefs. Mar. Ecol. Prog. Ser. 615, 1–14 (2019).ADS 
    Article 

    Google Scholar 
    Borgstein, N., Beltrán, D. M. & Prada, C. Variable growth across species and life stages in Caribbean reef octocorals. Front. Mar. Sci. 7, 483 (2020).Article 

    Google Scholar 
    Guizien, K. & Ghisalberti, M. in Marine Animal Forests: The Ecology of Benthic Biodiversity Hotspots (eds Rossi, S. et al.) 1–22 (Springer International Publishing, 2015).
    Google Scholar 
    Isbell, F. I., Polley, H. W. & Wilsey, B. J. Biodiversity, productivity and the temporal stability of productivity: patterns and processes. Ecol. Lett. 12, 443–451 (2009).PubMed 
    Article 

    Google Scholar 
    Simonson, W. D., Allen, H. D., Coomes, D. A. & Tatem, A. Applications of airborne lidar for the assessment of animal species diversity. Methods Ecol. Evol. 5, 719–729 (2014).Article 

    Google Scholar 
    Roscher, C. et al. Identifying population- and community-level mechanisms of diversity-stability relationships in experimental grasslands. J. Ecol. 99, 1460–1469 (2011).Article 

    Google Scholar 
    Yang, Z., Ruijven, V. J. & Du, G. The effects of long-term fertilization on the temporal stability of alpine meadow communities. Plant Soil 345, 315–324 (2011).CAS 
    Article 

    Google Scholar 
    Wilcox, K. R. et al. Asynchrony among local communities stabilises ecosystem function of metacommunities. Ecol. Lett. 20, 1534–1545 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rosenfeld, J. S. Logical fallacies in the assessment of functional redundancy. Conserv. Biol. 16, 837–839 (2002).Article 

    Google Scholar 
    Loreau, M. Does functional redundancy exist?. Oikos 104, 606–611 (2004).Article 

    Google Scholar 
    Gambrel, B. & Lasker, H. R. Interactions in the canopy among Caribbean reef octocorals. Mar. Ecol. Prog. Ser. 546, 85–95 (2016).ADS 
    Article 

    Google Scholar 
    Zambrano, J. et al. Tree crown overlap improves predictions of the functional neighbourhood effects on tree survival and growth. J. Ecol. 107, 887–900 (2019).Article 

    Google Scholar 
    Pescador, et al. 2018 The shape is more important than we ever thought: Plant to plant interactions in a high mountain community. Methods Ecol. Evol. 10, 1584–1593 (2019).Article 

    Google Scholar 
    Cerpovicz, A. F. & Lasker, H. R. Canopy effects of octocoral communities on sedimentation: modern baffles on the shallow-water reefs of St. John, USVI. Coral Reefs 40, 295 (2021).Article 

    Google Scholar 
    Martinez-Quintana, Á. & Lasker, H. R. Early life-history dynamics of Caribbean octocorals: the critical role of larval supply and partial mortality. Front. Mar. Sci. https://doi.org/10.3389/fmars.2021.705563 (2021).Article 

    Google Scholar 
    Tsounis, G., Steele, M. A. & Edmunds, P. J. Elevated feeding rates of fishes within octocoral canopies on Caribbean reefs. Coral Reefs 39, 1299–1311 (2020).Article 

    Google Scholar 
    Girard, J. & Edmunds, P.J. Effects of arborescent octocoral assemblages on the understory benthic communities of shallow Caribbean reefs. J. Exp. Mar. Biol. Ecol. (in review).Privitera-Johnson, K., Lenz, E. A. & Edmunds, P. J. Density-associated recruitment in octocoral communities in St. John, US Virgin Islands. J. Exp. Mar. Biol. Ecol. 473, 103–109. https://doi.org/10.1016/j.jembe.2015.08.006 (2015).Article 

    Google Scholar 
    Slattery, M. & Lesser, M. P. Gorgonians are foundation species on sponge-dominated Mesophotic Coral Reefs in the Caribbean. Front. Mar. Sci. https://doi.org/10.3389/fmars.2021.654268 (2021).Article 

    Google Scholar 
    Lasker, H. R. & Porto-Hannes, I. Population structure among octocoral adults and recruits identifies scale dependent patterns of population isolation in The Bahamas. PeerJ 3, e1019. https://doi.org/10.7717/peerj.1019 (2015).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Clark, D. A. & Clark, D. B. Getting to the canopy: tree height growth in a neotropical rain forest. Ecology 82, 1460–1472 (2001).Article 

    Google Scholar 
    Birkeland, C. Coral Reefs in the Anthropocene 1–15 (Springer, 2015).Book 

    Google Scholar 
    Petraitis, P. S. & Dudgeon, S. R. Cusps and butterflies: multiple stable states in marine systems as catastrophes. Mar. Freshw. Res. 67, 37–46 (2015).Article 

    Google Scholar  More

  • in

    Patterns and ecological drivers of viral communities in acid mine drainage sediments across Southern China

    Torsvik, V., Øvreås, L. & Thingstad, T. F. Prokaryotic diversity-magnitude, dynamics, and controlling factors. Science 296, 1064–1066 (2002).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Kuang, J. et al. Predicting taxonomic and functional structure of microbial communities in acid mine drainage. ISME J. 10, 1527–1539 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Mod, H. K. et al. Predicting spatial patterns of soil bacteria under current and future environmental conditions. ISME J. (2021).Pace, N. R. A molecular view of microbial diversity and the biosphere. Science 276, 734–740 (1997).CAS 
    PubMed 
    Article 

    Google Scholar 
    Violle, C., Reich, P. B., Pacala, S. W., Enquist, B. J. & Kattge, J. The emergence and promise of functional biogeography. Proc. Natl Acad. Sci. USA 111, 13690–13696 (2004).ADS 
    Article 
    CAS 

    Google Scholar 
    Green, J. L., Bohannan, B. J. & Whitaker, R. J. Microbial biogeography: from taxonomy to traits. Science 320, 1039–1043 (2008).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Daly, R. A. et al. Viruses control dominant bacteria colonizing the terrestrial deep biosphere after hydraulic fracturing. Nat. Microbiol. 4, 352–361 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Howard-Varona, C. et al. Phage-specific metabolic reprogramming of virocells. ISME J. 14, 881–895 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Chevallereau, A., Pons, B. J., van Houte, S. & Westra, E. R. Interactions between bacterial and phage communities in natural environments. Nat. Rev. Microbiol. 20, 49–62 (2022).CAS 
    PubMed 
    Article 

    Google Scholar 
    Sullivan, M. B., Weitz, J. S. & Wilhelm, S. Viral ecology comes of age. Environ. Microbiol. Rep. 9, 33–35 (2017).PubMed 
    Article 

    Google Scholar 
    Brum, J. R. & Sullivan, M. B. Rising to the challenge: accelerated pace of discovery transforms marine virology. Nat. Rev. Microbiol. 13, 147–159 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Roux, S. et al. Minimum information about an uncultivated virus genome (MIUViG). Nat. Biotechnol. 37, 29–37 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Brum, J. R. et al. Patterns and ecological drivers of ocean viral communities. Science 348, 1261498 (2015).PubMed 
    Article 
    CAS 

    Google Scholar 
    Gregory, A. C. et al. Marine DNA viral macro- and microdiversity from pole to pole. Cell 177, 1109–1123 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Shu, W. S. & Huang, L. N. Microbial diversity in extreme environments. Nat. Rev. Microbiol. (2021).Huang, L. N., Kuang, J. L. & Shu, W. S. Microbial ecology and evolution in the acid mine drainage model system. Trends Microbiol 24, 581–593 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hwang, Y., Rahlff, J., Schulze-Makuch, D., Schloter, M. & Probst, A. J. Diverse viruses carrying genes for microbial extremotolerance in the Atacama desert hyperarid soil. mSystems 6, e00385–21 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Adriaenssens, E. M. et al. Environmental drivers of viral community composition in Antarctic soils identified by viromics. Microbiome 5, 83 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Emerson, J. B. et al. Host-linked soil viral ecology along a permafrost thaw gradient. Nat. Microbiol. 3, 870–880 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Andersson, A. F. & Banfield, J. F. Virus population dynamics and acquired virus resistance in natural microbial communities. Science 320, 1047–1050 (2008).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Gao, S. M. et al. Depth-related variability in viral communities in highly stratified sulfidic mine tailings. Microbiome 8, 89 (2020).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Holmfeldt, K. et al. The Fennoscandian Shield deep terrestrial virosphere suggests slow motion ‘boom and burst’ cycles. Commun. Biol. 4, 307 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rahlff, J. et al. Lytic archaeal viruses infect abundant primary producers in Earth’s crust. Nat. Commun. 12, 4642 (2021).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hao, Y. Q. et al. Microbial biogeography of acid mine drainage sediments at a regional scale across Southern China. FEMS Microbiol. Ecol. 98, fiac002 (2022).PubMed 
    Article 

    Google Scholar 
    Paez-Espino, D., Pavlopoulos, G. A., Ivanova, N. N. & Kyrpides, N. C. Nontargeted virus sequence discovery pipeline and virus clustering for metagenomic data. Nat. Protoc. 12, 1673–1682 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Roux, S., Enault, F., Hurwitz, B. L. & Sullivan, M. B. VirSorter: mining viral signal from microbial genomic data. PeerJ 3, e985 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Nayfach, S. et al. CheckV: assessing the quality of metagenome-assembled viral genomes. Nat. Biotechnol. 39, 578–585 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bin Jang, H. et al. Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks. Nat. Biotechnol. 37, 632–639 (2019).Article 
    CAS 

    Google Scholar 
    Li, Z. et al. Deep sea sediments associated with cold seeps are a subsurface reservoir of viral diversity. ISME J. 15, (2021).Huerta-Cepas, J. et al. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res 47, D309–D314 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Wu, S. et al. DeePhage: distinguishing virulent and temperate phage-derived sequences in metavirome data with a deep learning approach. Gigascience 10, giab056 (2021).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Chen, L. X. et al. Comparative metagenomic and metatranscriptomic analyses of microbial communities in acid mine drainage. ISME J. 9, 1579–1592 (2015).PubMed 
    Article 

    Google Scholar 
    Liang, J. L. et al. Novel phosphate-solubilizing bacteria enhance soil phosphorus cycling following ecological restoration of land degraded by mining. ISME J. 14, 1600–1613 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hsieh, Y. J. & Wanner, B. L. Global regulation by the seven-component Pi signaling system. Curr. Opin. Microbiol. 13, 198–203 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Stasi, R., Neves, H. I. & Spira, B. Phosphate uptake by the phosphonate transport system PhnCDE. BMC Microbiol 19, 79 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Narr, A., Nawaz, A., Wick, L. Y., Harms, H. & Chatzinotas, A. Soil viral communities vary temporally and along a land use transect as revealed by virus-like particle counting and a modified community fingerprinting approach (fRAPD). Front. Microbiol. 8, 1975 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Santos-Medellin, C. et al. Viromes outperform total metagenomes in revealing the spatiotemporal patterns of agricultural soil viral communities. ISME J. 15, 1956–1970 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Tyson, G. W. & Banfield, J. F. Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses. Environ. Microbiol. 10, 200–207 (2008).CAS 
    PubMed 

    Google Scholar 
    Sun, C. L. et al. Phage mutations in response to CRISPR diversification in a bacterial population. Environ. Microbiol. 15, 463–470 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hurwitz, B. L., Westveld, A. H., Brum, J. R. & Sullivan, M. B. Modeling ecological drivers in marine viral communities using comparative metagenomics and network analyses. Proc. Natl Acad. Sci. USA 111, 10714–10719 (2014).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Jin, M. et al. Diversities and potential biogeochemical impacts of mangrove soil viruses. Microbiome 7, 58 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Dinsdale, E. A. et al. Functional metagenomic profiling of nine biomes. Nature 452, 629–632 (2008).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Tedersoo, L. et al. Fungal biogeography. Global diversity and geography of soil fungi. Science 346, 1256688 (2014).PubMed 
    Article 
    CAS 

    Google Scholar 
    Miraldo, A. et al. An Anthropocene map of genetic diversity. Science 353, 1532–1535 (2016).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Bonnain, C., Breitbart, M. & Buck, K. N. The Ferrojan horse hypothesis: iron-virus interactions in the ocean. Front. Mar. Sci. 3, 82 (2016).Article 

    Google Scholar 
    Muratore, D. & Weitz, J. S. Infect while the iron is scarce: nutrient-explicit phage-bacteria games. Theor. Ecol. 14, 467–487 (2021).Article 

    Google Scholar 
    Kyle, J. E., Pedersen, K. & Ferris, F. G. Virus mineralization at low pH in the Rio Tinto. Spain Geomicrobiol. J. 25, 338–345 (2008).CAS 
    Article 

    Google Scholar 
    Kyle, J. E. & Ferris, F. G. Geochemistry of virus–prokaryote interactions in freshwater and acid mine drainage environments, Ontario, Canada. Geomicrobiol. J. 30, 769–778 (2013).CAS 
    Article 

    Google Scholar 
    Hewson, I., O’Neil, J. M., Fuhrman, J. A. & Dennison, W. C. Virus-like particle distribution and abundance in sediments and overlying waters along eutrophication gradients in two subtropical estuaries. Limnol. Oceanogr. 46, 1734–1746 (2001).ADS 
    Article 

    Google Scholar 
    Wu, L. et al. Global diversity and biogeography of bacterial communities in wastewater treatment plants. Nat. Microbiol. 4, 1183–1195 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bates, S. T. et al. Global biogeography of highly diverse protistan communities in soil. ISME J. 7, 652–659 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Kuang, J. L. et al. Contemporary environmental variation determines microbial diversity patterns in acid mine drainage. ISME J. 7, 1038–1050 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Sant, D. G., Woods, L. C., Barr, J. J. & McDonald, M. J. Host diversity slows bacteriophage adaptation by selecting generalists over specialists. Nat. Ecol. Evol. 5, 350–359 (2021).PubMed 
    Article 

    Google Scholar 
    Betts, A., Gray, C., Zelek, M., MacLean, R. C. & King, K. C. High parasite diversity accelerates host adaptation and diversification. Science 360, 907–911 (2018).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Goldsmith, D. B., Parsons, R. J., Beyene, D., Salamon, P. & Breitbart, M. Deep sequencing of the viral phoH gene reveals temporal variation, depth-specific composition, and persistent dominance of the same viral phoH genes in the Sargasso Sea. Peer. J. 3, e997 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Goldsmith, D. B. et al. Development of phoH as a novel signature gene for assessing marine phage diversity. Appl. Environ. Microbiol. 77, 7730–7739 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Martiny, A. C., Coleman, M. L. & Chisholm, S. W. Phosphate acquisition genes in Prochlorococcus ecotypes: evidence for genome-wide adaptation. Proc. Natl Acad. Sci. USA 103, 12552–12557 (2006).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Tetu, S. G. et al. Microarray analysis of phosphate regulation in the marine cyanobacterium Synechococcus sp. WH8102. ISME J. 3, 835–849 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    Zeng, Q. & Chisholm, S. W. Marine viruses exploit their host’s two-component regulatory system in response to resource limitation. Curr. Biol. 22, 124–128 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Kazakov, A. E., Vassieva, O., Gelfand, M. S., Osterman, A. & Overbeek, R. Bioinformatics classification and functional analysis of PhoH homologs. Silico Biol. 3, 3–15 (2003).CAS 

    Google Scholar 
    Bray, R. H. & Kurtz, L. T. Determination of total, organic, and available forms of phosphorus in soils. Soil Sci. 59, 39–46 (1945).ADS 
    CAS 
    Article 

    Google Scholar 
    Hill, A. G. et al. Standardized general method for the determination of iron with 1,10-phenanthroline. Analyst 103, 391–396 (1978).Article 

    Google Scholar 
    Chesmin, L. & Yien, C. H. Turbidimetric determination of available sulphate. Soil Sci. Soc. Am. Proc. 15, 149–151 (1951).ADS 
    Article 

    Google Scholar 
    Fang, Y. et al. Modified pretreatment method for total microbial DNA extraction from contaminated river sediment. Front. Environ. Sci. Eng. 9, 444–452 (2015).CAS 
    Article 

    Google Scholar 
    Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2012).MathSciNet 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hyatt, D. et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinforma. 11, 119 (2010).Article 
    CAS 

    Google Scholar 
    El-Gebali, S. et al. The Pfam protein families database in 2019. Nucleic Acids Res 47, D427–D432 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Kanehisa, M., Sato, Y., Kawashima, M., Furumichi, M. & Tanabe, M. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res 44, D457–D462 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Eddy, S. R. Accelerated profile HMM searches. PLOS Comput. Biol. 7, e1002195 (2011).ADS 
    MathSciNet 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Roux, S., Hallam, S. J., Woyke, T. & Sullivan, M. B. Viral dark matter and virus-host interactions resolved from publicly available microbial genomes. Elife 4, e08490 (2015).PubMed Central 
    Article 

    Google Scholar 
    Roux, S. et al. Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature 537, 689–693 (2016).CAS 
    PubMed 
    Article 

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

    Google Scholar 
    Kang, D. D. et al. MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies. PeerJ 7, e7359 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Wu, Y. W., Simmons, B. A. & Singer, S. W. MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets. Bioinformatics 32, 605–607 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Brown, C. T. et al. Unusual biology across a group comprising more than 15% of domain Bacteria. Nature 523, 208–201 (2015).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Alneberg, J. et al. Binning metagenomic contigs by coverage and composition. Nat. Methods 11, 1144–1146 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    Sieber, C. M. K. et al. Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy. Nat. Microbiol. 3, 836–843 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Parks, D. H. et al. Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nat. Microbiol. 2, 1533–1542 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Chaumeil, P. A., Mussig, A. J., Hugenholtz, P. & Parks, D. H. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics 36, 1925–1927 (2019).PubMed Central 

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

    Google Scholar 
    Woodcroft, B. J. et al. Genome-centric view of carbon processing in thawing permafrost. Nature 560, 49–54 (2018).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Edwards, R. A., McNair, K., Faust, K., Raes, J. & Dutilh, B. E. Computational approaches to predict bacteriophage-host relationships. FEMS Microbiol. Rev. 40, 258–272 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Rho, M., Wu, Y. W., Tang, H., Doak, T. G. & Ye, Y. Diverse CRISPRs evolving in human microbiomes. PLoS Genet. 8, e1002441 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Paez-Espino, D. et al. Uncovering Earth’s virome. Nature 536, 425–430 (2016).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Edgar, R. C. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinforma. 5, 113 (2004).Article 
    CAS 

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

    Google Scholar 
    Minh, B. Q. et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530–1534 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 47, W256–W259 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    R Development Core Team. R: A Language and environment for statistical computing. (2013).Oksanen, J. et al. vegan: Community ecology package. R package version 2.5-5. (2019).Harrell, F. E. Jr. & Dupont, M. C. The hmisc package. R. package version 4, 2–0 (2019).
    Google Scholar 
    R Development Core Team. The R Stats Package. R package version 4.0.3 (2013).Rosseel, Y. Lavaan: An R package for structural equation modeling and more. Version 0.5-12 (BETA). J. Stat. Soft 48, 1–36 (2012).Article 

    Google Scholar 
    Flores, C. O., Meyer, J. R., Valverde, S., Farr, L. & Weitz, J. S. Statistical structure of host-phage interactions. Proc. Natl Acad. Sci. USA 108, E288–E297 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

  • in

    Limits to reproduction and seed size-number trade-offs that shape forest dominance and future recovery

    Curtis, P. G., Slay, C. M., Harris, N. L., Tyukavina, A. & Hansen, M. C. Classifying drivers of global forest loss. Science 361, 1108–1111 (2018).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Duane, A., Castellnou, M. & Brotons, L. Towards a comprehensive look at global drivers of novel extreme wildfire events. Clim. Change 165, 43 (2021).ADS 
    Article 

    Google Scholar 
    Allen, C. D. et al. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For. Ecol. Manag. 259, 660–684 (2010). Adaptation of Forests and Forest Management to Changing Climate.Article 

    Google Scholar 
    Franklin, J. F., Mitchell, R. J. & Palik, B. J. Natural disturbance and stand development principles for ecological forestry. General Technical Report. NRS-19. Newtown Square, PA: US Department of Agriculture, Forest Service, Northern Research Station. 44. p. 19 (2007).Westoby, M., Jurado, E. & Leishman, M. Comparative evolutionary ecology of seed size. Trends Ecol. Evol. 7, 368–372 (1992).CAS 
    PubMed 
    Article 

    Google Scholar 
    Smith, C. C. & Fretwell, S. D. The optimal balance between size and number of offspring. Am. Nat. 108, 499–506 (1974).Article 

    Google Scholar 
    Lord, J., Westoby, M. & Leishman, M. Seed size and phylogeny in six temperate floras: Constraints, niche conservatism, and adaptation. Am. Nat. 146, 349–364 (1995).Article 

    Google Scholar 
    Moles, A. T. et al. Global patterns in seed size. Glob. Ecol. Biogeogr. 16, 109–116 (2007).Article 

    Google Scholar 
    Tautenhahn, S. et al. On the biogeography of seed mass in germany – distribution patterns and environmental correlates. Ecography 31, 457–468 (2008).Article 

    Google Scholar 
    Lidgard, S. & Crane, P. R. Quantitative analyses of the early angiosperm radiation. Nature 331, 344–346 (1988).ADS 
    Article 

    Google Scholar 
    Crisp, M. D. & Cook, L. G. Cenozoic extinctions account for the low diversity of extant gymnosperms compared with angiosperms. New Phytol. 192, 997–1009 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    Stearns, S. C. Life-history tactics: a review of the ideas. Quart. Rev. Biol. 51, 3–47 (1976).CAS 
    PubMed 
    Article 

    Google Scholar 
    Grubb, P. J. The maintenance of species-richness in plant communities: the importance of the regeneration niche. Biol. Rev. 52, 107–145 (1977).Article 

    Google Scholar 
    Clark, J. S., LaDeau, S. & Ibanez, I. Fecundity of trees and the colonization-competition hypothesis. Ecol. Monogr. 74, 415–442 (2004).Article 

    Google Scholar 
    Salguero-Gómez, R. et al. Fast-slow continuum and reproductive strategies structure plant life-history variation worldwide. Proc. Natl Acad. Sci. USA 113, 230–235 (2016).ADS 
    PubMed 
    Article 
    CAS 

    Google Scholar 
    Thomas, S. C. Age-Related Changes in Tree Growth and Functional Biology: The Role of Reproduction, p. 33-64 (Springer Netherlands, 2011).Wenk, E. H. & Falster, D. S. Quantifying and understanding reproductive allocation schedules in plants. Ecol. Evol. 5, 5521–5538 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bar-On, Y. M., Phillips, R. & Milo, R. The biomass distribution on earth. Proc. Natl Acad. Sci. USA 115, 6506–6511 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Turnbull, L. A., Rees, M. & Crawley, M. J. Seed mass and the competition/colonization trade-off: a sowing experiment. J. Ecol. 87, 899–912 (1999).Article 

    Google Scholar 
    Moles, A., Falster, D., Leishman, M. & Westoby, M. Small-seeded species produce more seeds per square metre of canopy per year, but not per individual per lifetime. J. Ecol. 92, 384–396 (2004).Article 

    Google Scholar 
    Qiu, T. et al. Is there tree senescence? the fecundity evidence. Proc. Natl Acad. Sci. USA 118, e2106130118 (2021).Westoby, M., Falster, D. S., Moles, A. T., Vesk, P. A. & Wright, I. J. Plant ecological strategies: Some leading dimensions of variation between species. Annu. Rev. Ecol. Syst. 33, 125–159 (2002).Article 

    Google Scholar 
    Henery, M. L. & Westoby, M. Seed mass and seed nutrient content as predictors of seed output variation between species. Oikos 92, 479–490 (2001).Article 

    Google Scholar 
    Turnbull, L. A., Coomes, D., Hector, A. & Rees, M. Seed mass and the competition/colonization trade-off: competitive interactions and spatial patterns in a guild of annual plants. J. Ecol. 92, 97–109 (2004).Article 

    Google Scholar 
    Chave, J. et al. Towards a worldwide wood economics spectrum. Ecol. Lett. 12, 351–366 (2009).PubMed 
    Article 

    Google Scholar 
    Poorter, L. et al. The importance of wood traits and hydraulic conductance for the performance and life history strategies of 42 rainforest tree species. New Phytol. 185, 481–492 (2010).PubMed 
    Article 

    Google Scholar 
    Hanley, M. E., Cook, B. I. & Fenner, M. Climate variation, reproductive frequency and acorn yield in english oaks. J. Plant Ecol. 12, 542–549 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kattge, J. et al. Try plant trait database – enhanced coverage and open access. Glob. Change Biol. 26, 119–188 (2020).ADS 
    Article 

    Google Scholar 
    Ran, E., Arnon, D., Alon, B.-G., Amnon, S. & Uri, Y. Flowering and fruit set of olive trees in response to nitrogen, phosphorus, and potassium. J. Am. Soc. Hortic. Sci. Am. Soc. Hortic. Sci. 133, 639–647 (2008).Article 

    Google Scholar 
    Fernández-Martínez, M., Vicca, S., Janssens, I. A., Espelta, J. M. & Peñuelas, J. The role of nutrients, productivity and climate in determining tree fruit production in european forests. New Phytol. 213, 669–679 (2017).PubMed 
    Article 
    CAS 

    Google Scholar 
    Fortier, R. & Wright, S. J. Nutrient limitation of plant reproduction in a tropical moist forest. Ecology 102, e03469 (2021).Canham, C. D., Ruscoe, W. A., Wright, E. F. & Wilson, D. J. Spatial and temporal variation in tree seed production and dispersal in a new zealand temperate rainforest. Ecosphere 5, art49 (2014).Article 

    Google Scholar 
    Pérez-Ramos, I. M., Aponte, C., García, L. V., Padilla-Díaz, C. M. & Marañón, T. Why is seed production so variable among individuals? a ten-year study with oaks reveals the importance of soil environment. PLoS ONE 9, e115371 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Sitch, S. et al. Evaluation of ecosystem dynamics, plant geography and terrestrial carbon cycling in the LPJ dynamic global vegetation model. Glob. Change Biol. 9, 161–185 (2003).ADS 
    Article 

    Google Scholar 
    Krinner, G. et al. A dynamic global vegetation model for studies of the coupled atmosphere-biosphere system. Glob. Biogeochem. Cycles 19, 1–33 (2005).Article 
    CAS 

    Google Scholar 
    Fisher, R. A. et al. Vegetation demographics in earth system models: a review of progress and priorities. Glob. Change Biol. 24, 35–54 (2018).ADS 
    Article 

    Google Scholar 
    Hanbury-Brown, A., Ward, R. & Kueppers, L. M. Future forests within earth system models: regeneration processes critical to prediction. New Phytol. in press https://doi.org/10.1111/nph.18131 (2022).Stiles, W. C. & Reid, W. S. Orchard nutrition management. Inf. Bull. (1991). https://ecommons.cornell.edu/bitstream/handle/1813/3305/Orchard%20Nutrition%20Management.pdf?sequence=2&isAllowed=y.Schlesinger, W. H. Some thoughts on the biogeochemical cycling of potassium in terrestrial ecosystems. Biogeochemistry 154, 427–432 (2021).Article 

    Google Scholar 
    Neilsen, D. & Neilsen, G. Efficient use of nitrogen and water in high-density apple orchards. HortTechnology 12, 19 (2002).Article 

    Google Scholar 
    Rubio Ames, Z., Brecht, J. K. & Olmstead, M. A. Nitrogen fertilization rates in a subtropical peach orchard: effects on tree vigor and fruit quality. J. Sci. Food Agric. 100, 527–539 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Elser, J. J. et al. Growth rate-stoichiometry couplings in diverse biota. Ecol. Lett. 6, 936–943 (2003).Article 

    Google Scholar 
    Seyednasrollah, B. & Clark, J. S. Where resource-acquisitive species are located: the role of habitat heterogeneity. Geophys. Res. Lett. 47, e2020GL087626 (2020).Rosecrance, R. C., Weinbaum, S. A. & Brown, P. H. Alternate bearing affects nitrogen, phosphorus, potassium and starch storage pools in mature pistachio trees. Ann. Bot. 82, 463–470 (1998).Article 

    Google Scholar 
    Sala, A., Hopping, K., McIntire, E. J. B., Delzon, S. & Crone, E. E. Masting in whitebark pine (pinus albicaulis) depletes stored nutrients. New Phytol. 196, 189–199 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    LaDeau, S. L. & Clark, J. S. Rising co2 levels and the fecundity of forest trees. Science 292, 95–8 (2001).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Callahan, H. S., Del Fierro, K., Patterson, A. E. & Zafar, H. Impacts of elevated nitrogen inputs on oak reproductive and seed ecology. Glob. Change Biol. 14, 285–293 (2008).ADS 
    Article 

    Google Scholar 
    Lambers, H. & Poorter, H. Inherent Variation in Growth Rate Between Higher Plants: A Search for Physiological Causes and Ecological Consequences, vol. 23, 187-261 (Academic Press, 1992).Hengl, T. et al. Soilgrids250m: global gridded soil information based on machine learning. PLoS ONE 12, 1–40 (2017).Article 
    CAS 

    Google Scholar 
    Sharma, A., Weindorf, D. C., Wang, D. D. & Chakraborty, S. Characterizing soils via portable x-ray fluorescence spectrometer: 4. cation exchange capacity (cec). Geoderma 239, 130–134 (2015).ADS 
    Article 
    CAS 

    Google Scholar 
    Hazelton, P. & Murphy, B. Interpreting Soil Test Results: What Do All The Numbers Mean? (CSIRO publishing, 2016).Chowdhury, S. et al. Chapter Two – Role Of Cultural And Nutrient Management Practices In Carbon Sequestration In Agricultural Soil, vol. 166, 131-196 (Academic Press, 2021).Clark, J. S., Nuñez, C. L. & Tomasek, B. Foodwebs based on unreliable foundations: spatiotemporal masting merged with consumer movement, storage, and diet. Ecol. Monogr. 89, e01381 (2019).Article 

    Google Scholar 
    Burns, R. M. Silvics Of North America (US Department of Agriculture, Forest Service, 1990).Koenig, W. D. & Knops, J. M. H. Seed-crop size and eruptions of north american boreal seed-eating birds. J. Anim. Ecol. 70, 609–620 (2001).Article 

    Google Scholar 
    Greene, D. F. & Johnson, E. A. Estimating the mean annual seed production of trees. Ecology 75, 642–647 (1994).Article 

    Google Scholar 
    Lord, J. M. & Westoby, M. Accessory costs of seed production and the evolution of angiosperms. Evol. Int. J. Org. Evol. 66, 200–210 (2012).Article 

    Google Scholar 
    Hulme, P. & Benkman, C. Granivory. vol. 23, 132-154 (Oxford: Blackwell, 2002).Bond, W. J. The tortoise and the hare: ecology of angiosperm dominance and gymnosperm persistence. Biol. J. Linn. Soc. 36, 227–249 (1989).Article 

    Google Scholar 
    Brodribb, T. J. & Feild, T. S. Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecol. Lett. 13, 175–183 (2010).PubMed 
    Article 

    Google Scholar 
    Davies, T. J. et al. Darwin’s abominable mystery: Insights from a supertree of the angiosperms. Proc. Natl Acad. Sci. USA 101, 1904–1909 (2004).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Berendse, F. & Scheffer, M. The angiosperm radiation revisited, an ecological explanation for darwin’s ‘abominable mystery’. Ecol. Lett. 12, 865–872 (2009).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Barrett, S. C. H. Influences of clonality on plant sexual reproduction. Proc. Natl Acad. Sci. USA 112, 8859–8866 (2015).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Condamine, F. L., Silvestro, D., Koppelhus, E. B. & Antonelli, A. The rise of angiosperms pushed conifers to decline during global cooling. Proc. Natl Acad. Sci. USA 117, 28867–28875 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Oren, R. et al. Soil fertility limits carbon sequestration by forest ecosystems in a co2-enriched atmosphere. Nature 411, 469–472 (2001).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Reich, P. B. et al. Nitrogen limitation constrains sustainability of ecosystem response to co2. Nature 440, 922–925 (2006).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Firn, J. et al. Leaf nutrients, not specific leaf area, are consistent indicators of elevated nutrient inputs. Nat. Ecol. Evol. 3, 400–406 (2019).PubMed 
    Article 

    Google Scholar 
    Elser, J. et al. Biological stoichiometry from genes to ecosystems. Ecol. Lett. 3, 540–550 (2000).Article 

    Google Scholar 
    Niklas, K. J., Owens, T., Reich, P. B. & Cobb, E. D. Nitrogen/phosphorus leaf stoichiometry and the scaling of plant growth. Ecol. Lett. 8, 636–642 (2005).Article 

    Google Scholar 
    Kerkhoff, A. J., Fagan, W. F., Elser, J. J. & Enquist, B. J. Phylogenetic and growth form variation in the scaling of nitrogen and phosphorus in the seed plants. Am. Nat. 168, E103–E122 (2006).PubMed 
    Article 

    Google Scholar 
    Weinbaum, S. A., Johnson, R. S. & DeJong, T. M. Causes and consequences of overfertilization in orchards. HortTechnology 2, 112b (1992).Article 

    Google Scholar 
    Fernandez-Escobar, R. et al. Olive oil quality decreases with nitrogen over-fertilization. HortScience 41, 215 (2006).CAS 
    Article 

    Google Scholar 
    Han, Q., Kabeya, D., Iio, A. & Kakubari, Y. Masting in fagus crenata and its influence on the nitrogen content and dry mass of winter buds. Tree Physiol. 28, 1269–1276 (2008).PubMed 
    Article 

    Google Scholar 
    Pettigrew, W. T. Potassium influences on yield and quality production for maize, wheat, soybean and cotton. Physiol. Plant. 133, 670–681 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    Leeper, A. C., Lawrence, B. A. & LaMontagne, J. M. Plant-available soil nutrients have a limited influence on cone production patterns of individual white spruce trees. Oecologia 194, 101–111 (2020).ADS 
    PubMed 
    Article 

    Google Scholar 
    Chapin, F. S., Autumn, K. & Pugnaire, F. Evolution of suites of traits in response to environmental stress. Am. Nat. 142, S78–S92 (1993).Article 

    Google Scholar 
    Westoby, M. & Wright, I. J. Land-plant ecology on the basis of functional traits. Trends Ecol. Evol. 21, 261–268 (2006).PubMed 
    Article 

    Google Scholar 
    Brodribb, T. J., Pittermann, J. & Coomes, D. A. Elegance versus speed: Examining the competition between conifer and angiosperm trees. Int. J. Plant Sci. 173, 673–694 (2012).Article 

    Google Scholar 
    Clark, J. S., Macklin, E. & Wood, L. Stages and spatial scales of recruitment limitation in southern appalachian forests. Ecol. Monogr. 68, 213–235 (1998).Article 

    Google Scholar 
    McEuen, A. B. & Curran, L. M. Seed dispersal and recruitment limitation across spatial scales in temperate forest fragments. Ecology 85, 507–518 (2004).Article 

    Google Scholar 
    Emsweller, L. N., Gorchov, D. L., Zhang, Q., Driscoll, A. G. & Hughes, M. R. Seed rain and disturbance impact recruitment of invasive plants in upland forest. Invasive Plant Sci. Manag. 11, 69–81 (2018).Article 

    Google Scholar 
    Lindgren, s, Eriksson, O. & Moen, J. The impact of disturbance and seed availability on germination of alpine vegetation in the scandinavian mountains. Arct. Antarct. Alp. Res. 39, 449–454 (2007).Article 

    Google Scholar 
    Cai, W. H., Liu, Z., Yang, Y. Z. & Yang, J. Does environment filtering or seed limitation determine post-fire forest recovery patterns in boreal larch forests? Front. Plant Sci. 9, 1318 (2018).Darwin, C. On the Origin of Species (John Murray, 1859).Black, M. Darwin and seeds. Seed Sci. Res. 19, 193–199 (2009).Article 

    Google Scholar 
    FAO. Global forest resources assessment 2020-key findings. un food and agriculture organization. Report (2020).Payn, T. et al. Changes in planted forests and future global implications. For. Ecol. Manag. 352, 57–67 (2015).Article 

    Google Scholar 
    Clark, J. S. et al. The impacts of increasing drought on forest dynamics, structure, and biodiversity in the united states. Glob. Change Biol. 22, 2329–2352 (2016).ADS 
    Article 

    Google Scholar 
    Gazol, A., Camarero, J. J., Anderegg, W. R. L. & Vicente-Serrano, S. M. Impacts of droughts on the growth resilience of northern hemisphere forests. Glob. Ecol. Biogeogr. 26, 166–176 (2017).Article 

    Google Scholar 
    Stephens, S. L. et al. Managing forests and fire in changing climates. Science 342, 41–42 (2013).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    North, M. P. et al. Tamm review: reforestation for resilience in dry western u.s. forests. For. Ecol. Manag. 432, 209–224 (2019).Article 

    Google Scholar 
    Seidl, R., Rammer, W. & Spies, T. A. Disturbance legacies increase the resilience of forest ecosystem structure, composition, and functioning. Ecol. Appl. 24, 2063–2077 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Serra-Diaz, J. M. et al. Averaged 30 year climate change projections mask opportunities for species establishment. Ecography 39, 844–845 (2016).Article 

    Google Scholar 
    Davis, F. W. et al. Shrinking windows of opportunity for oak seedling establishment in southern california mountains. Ecosphere 7, e01573 (2016).
    Google Scholar 
    LeBauer, D. S. & Treseder, K. K. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89, 371–379 (2008).PubMed 
    Article 

    Google Scholar 
    Clark, J. S. et al. Continent-wide tree fecundity driven by indirect climate effects. Nat. Commun. 12, 1242 (2021).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Brady, N. C., Weil, R. R. & Weil, R. R. The Nature And Properties Of Soils, vol. 13 (Prentice Hall Upper Saddle River, 2008).Farr, T. G. et al. The shuttle radar topography mission. Rev. Geophys. 45, RG2004 (2007). https://doi.org/10.1029/2005RG000183.Clark, J. S. Landscape interactions among nitrogen mineralization, species composition, and long-term fire frequency. Biogeochemistry 11, 1–22 (1990).Article 

    Google Scholar 
    Clark, J. S., Bell, D. M., Kwit, M. C. & Zhu, K. Competition-interaction landscapes for the joint response of forests to climate change. Glob. Change Biol. 20, 1979–1991 (2014).ADS 
    Article 

    Google Scholar 
    Begueria, S., Vicente-Serrano, S. M., Reig, F. & Latorre, B. Standardized precipitation evapotranspiration index (spei) revisited: parameter fitting, evapotranspiration models, tools, datasets and drought monitoring. Int. J. Climatol. 34, 3001–3023 (2014).Article 

    Google Scholar 
    Abatzoglou, J. T., Dobrowski, S. Z., Parks, S. A. & Hegewisch, K. C. Terraclimate, a high-resolution global dataset of monthly climate and climatic water balance from 1958-2015. Sci. Data 5, 170191 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Karger, D. N. et al. Climatologies at high resolution for the earth’s land surface areas. Sci. Data 4, 170122 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Schneider, R., Calama, R. & Martin-Ducup, O. Understanding tree-to-tree variations in stone pine (pinus pinea l.) cone production using terrestrial laser scanner. Remote Sens. 12, 173 (2020).Article 

    Google Scholar 
    Gavranović, A., Bogdan, S., Lanšćak, M., Čehulić, I. & Ivanković, M. Seed yield and morphological variations of beechnuts in four european beech (fagus sylvatica l.) populations in croatia. South-East Eur. For. 9, 17–27 (2018).Article 

    Google Scholar 
    Maitner, B. S. et al. The bien r package: a tool to access the botanical information and ecology network (bien) database. Methods Ecol. Evol. 9, 373–379 (2018).Article 

    Google Scholar 
    Clark, J. S., Silman, M., Kern, R., Macklin, E. & HilleRisLambers, J. Seed dispersal near and far: patterns across temperate and tropical forests. Ecology 80, 1475–1494 (1999).Article 

    Google Scholar 
    LePage, P. T., Canham, C. D., Coates, K. D. & Bartemucci, P. Seed abundance versus substrate limitation of seedling recruitment in northern temperate forests of british columbia. Can. J. For. Res. 30, 415–427 (2000).Article 

    Google Scholar 
    Clark, J. S., LaDeau, S. & Ibanez, I. Fecundity of trees and the colonization-competition hypothesis. Ecol. Monogr. 74, 415–442 (2004).Article 

    Google Scholar 
    Muller-Landau, H. C., Wright, S. J., Calderon, O., Condit, R. & Hubbell, S. P. Interspecific variation in primary seed dispersal in a tropical forest. J. Ecol. 96, 653–667 (2008).Article 

    Google Scholar 
    Jones, F. A. & Muller-Landau, H. C. Measuring long-distance seed dispersal in complex natural environments: an evaluation and integration of classical and genetic methods. J. Ecol. 96, 642–652 (2008).Article 

    Google Scholar 
    Clark, J. S. Individuals and the variation needed for high species diversity in forest trees. Science 327, 1129–1132 (2010).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Clark, J. S. et al. High-dimensional coexistence based on individual variation: a synthesis of evidence. Ecol. Monogr. 80, 569–608 (2010).Article 

    Google Scholar 
    Clark, J. S., Bell, D. M., Kwit, M. C. & Zhu, K. Competition-interaction landscapes for the joint response of forests to climate change. Glob. Change Biol. 20, 1979–91 (2014).ADS 
    Article 

    Google Scholar 
    Minor, D. M. & Kobe, R. K. Fruit production is influenced by tree size and size-asymmetric crowding in a wet tropical forest. Ecol. Evol. 9, 1458–1472 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Zanne, A. E. et al. Three keys to the radiation of angiosperms into freezing environments. Nature 506, 89–92 (2014).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Pagel, M. Inferring the historical patterns of biological evolution. Nature 401, 877–884 (1999).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Revell, L. J. phytools: an r package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).Article 

    Google Scholar 
    Felsenstein, J. Phylogenies and the comparative method. Am. Nat. 125, 1–15 (1985).Article 

    Google Scholar 
    Martins, E. P. & Hansen, T. F. Phylogenies and the comparative method: A general approach to incorporating phylogenetic information into the analysis of interspecific data. Am. Nat. 149, 646–667 (1997).Article 

    Google Scholar 
    Tung Ho, L. S. & Ané, C. A linear-time algorithm for gaussian and non-gaussian trait evolution models. Syst. Biol. 63, 397–408 (2014).Article 

    Google Scholar 
    Clark, J. S. Data from: continent-wide tree fecundity driven by indirect climate effects https://doi.org/10.7924/r4348ph5t (2020). More