Philippa Kaur

World Health Organization. World malaria report 2022. (2022).Kariuki, S. N. & Williams, T. N. Human genetics and malaria resistance. Hum. Gen. 139, 801–811 (2020).Article 

Google Scholar 
Watson, J. A., White, N. J. & Dondorp, A. M. Falciparum malaria mortality in sub-Saharan Africa in the pretreatment era. Trends Parasitol. 38, 11–14 (2022).Article 
CAS 
PubMed 

Google Scholar 
Sanchez-Mazas, A. A review of HLA allele and SNP associations with highly prevalent infectious diseases in human populations. Swiss Med. Wkly. 150, w20214 (2020).PubMed 

Google Scholar 
Heijmans, C. M. C., de Groot, N. G. & Bontrop, R. E. Comparative genetics of the major histocompatibility complex in humans and nonhuman primates. Int. J. Immunogenet. 47, 243–260 (2020).Article 
CAS 
PubMed 

Google Scholar 
Neefjes, J., Jongsma, M. L., Paul, P. & Bakke, O. Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat. Rev. Immunol. 11, 823–836 (2011).Article 
CAS 
PubMed 

Google Scholar 
Zinkernagel, R. M. & Doherty, P. C. Restriction of in vitro T cell-mediated cytotoxicity in lymphocytic choriomeningitis within a syngeneic or semiallogeneic system. Nature 248, 701–702 (1974).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Colonna, M. & Samaridis, J. Cloning of Immunoglobulin-Superfamily Members Associated with HLA-C and HLA-B Recognition by Human Natural Killer Cells. Science 268, 405–408 (1995).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Hill, A. V. et al. Common west African HLA antigens are associated with protection from severe malaria. Nature 352, 595–600 (1991).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Sanchez‐Mazas, A. et al. The HLA‐B landscape of Africa: signatures of pathogen‐driven selection and molecular identification of candidate alleles to malaria protection. Mol. Ecol. 26, 6238–6252 (2017).Article 
PubMed 

Google Scholar 
Hill, A. V. et al. Molecular analysis of the association of HLA-B53 and resistance to severe malaria. Nature 360, 434–439 (1992).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Norman, P. J. et al. Co-evolution of human leukocyte antigen (HLA) class I ligands with killer-cell immunoglobulin-like receptors (KIR) in a genetically diverse population of sub-Saharan Africans. PLoS Genet. 9, e1003938 (2013).Article 
PubMed 
PubMed Central 

Google Scholar 
Sharp, P. M., Plenderleith, L. J. & Hahn, B. H. Ape origins of human malaria. Annu. Rev. Microbiol. 74, 39–63 (2020).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Liu, W. et al. Wild bonobos host geographically restricted malaria parasites including a putative new Laverania species. Nat. Commun. 8, 1635 (2017).Liu, W. et al. African origin of the malaria parasite Plasmodium vivax. Nat. Commun. 5, 3346 (2014).Article 
ADS 
PubMed 

Google Scholar 
Liu, W. et al. Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 467, 420–425 (2010).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Liu, W. et al. Multigenomic delineation of Plasmodium species of the Laverania subgenus infecting wild-living chimpanzees and gorillas. Genome Biol. Evol. 8, 1929–1939 (2016).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
De Nys, H. M. et al. Age-related effects on malaria parasite infection in wild chimpanzees. Biol. Lett. 9, 20121160 (2013).Article 
PubMed 
PubMed Central 

Google Scholar 
De Nys, H. M. et al. Malaria parasite detection increases during pregnancy in wild chimpanzees. Malar. J. 13, 1–6 (2014).
Google Scholar 
Mapua, M. I. et al. Ecology of malaria infections in western lowland gorillas inhabiting Dzanga Sangha Protected Areas, Central African Republic. Parasitology 142, 890–900 (2015).Article 
PubMed 

Google Scholar 
Scully, E. J. et al. The ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs. Commun. Biol. 5, 1020 (2022).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Herbert, A. et al. Malaria-like symptoms associated with a natural Plasmodium reichenowi infection in a chimpanzee. Malar. J. 14, 1–8 (2015).Article 

Google Scholar 
De Nys, H. M., Löhrich, T., Wu, D., Calvignac-Spencer, S. & Leendertz, F. H. Wild African great apes as natural hosts of malaria parasites: current knowledge and research perspectives. Primate Biol. 4, 47–59 (2017).Article 
PubMed 
PubMed Central 

Google Scholar 
Takemoto, H., Kawamoto, Y. & Furuichi, T. How did bonobos come to range south of the congo river? Reconsideration of the divergence of Pan paniscus from other Pan populations. Evol. Anthropol. 24, 170–184 (2015).Article 
PubMed 

Google Scholar 
Takemoto, H., Kawamoto, Y. & Furuichi, T. The formation of Congo River and the origin of bonobos: A new hypothesis. in Bonobos: unique in mind, brain, and behavior (eds. Hare, B. & Yamamoto, S.) 235-248 (Oxford University Press, 2017).Takemoto, H. et al. The mitochondrial ancestor of bonobos and the origin of their major haplogroups. PLoS One. 12, e0174851 (2017).Article 
PubMed 
PubMed Central 

Google Scholar 
Pilbrow, V. & Groves, C. Evidence for divergence in populations of bonobos (Pan paniscus) in the Lomami-Lualaba and Kasai-Sankuru regions based on preliminary analysis of craniodental variation. Int. J. Primatol. 34, 1244–1260 (2013).Article 

Google Scholar 
de Groot, N. G., Stevens, J. M. & Bontrop, R. E. Does the MHC confer protection against malaria in bonobos? Trends Immunol. 39, 768–771 (2018).Article 
PubMed 

Google Scholar 
Sidney, J., Peters, B., Frahm, N., Brander, C. & Sette, A. HLA class I supertypes: a revised and updated classification. BMC Immunol. 9, 1 (2008).Article 
PubMed 
PubMed Central 

Google Scholar 
Wroblewski, E. E. et al. Bonobos maintain immune system diversity with three functional types of MHC-B. J. Immunol. 198, 3480–3493 (2017).Article 
CAS 
PubMed 

Google Scholar 
Bjorkman, P. et al. The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature 329, 512–518 (1987).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Guethlein, L. A., Norman, P. J., Hilton, H. G. & Parham, P. Co-evolution of MHC class I and variable NK cell receptors in placental mammals. Immunol. Rev. 267, 259–282 (2015).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Wroblewski, E. E. et al. Signature patterns of MHC diversity in three Gombe communities of wild chimpanzees reflect fitness in reproduction and immune defense against SIVcpz. PLoS. Biol. 13, e1002144 (2015).Article 
PubMed 
PubMed Central 

Google Scholar 
Li, Y. et al. Eastern chimpanzees, but not bonobos, represent a simian immunodeficiency virus reservoir. J. Virol. 18, 10776–10791 (2012).Article 

Google Scholar 
Yang, C. et al. Sequence variations in the non-repetitive regions of the liver stage-specific antigen-1 (LSA-1) of Plasmodium falciparum from field isolates,. Mol. Biochem Parasitol. 71, 291–294 (1995).Article 
CAS 
PubMed 

Google Scholar 
Fidock, D. A. et al. Plasmodium falciparum liver stage antigen-1 is well conserved and contains potent B and T cell determinants. J. Immunol. 153, 190–204 (1994).Article 
CAS 
PubMed 

Google Scholar 
Aurrecoechea, C. et al. PlasmoDB: a functional genomic database for malaria parasites. Nucl. Acids Res. 37, D539–D543 (2009).Article 
CAS 
PubMed 

Google Scholar 
Hughes, A. L. & Yeager, M. Natural selection at major histocompatibility complex loci of vertebrates. Annu. Rev. Genet. 32, 415–435 (1998).Article 
CAS 
PubMed 

Google Scholar 
Trowsdale, J. The MHC, disease and selection. Immunol. Lett. 137, 1–8 (2011).Article 
CAS 
PubMed 

Google Scholar 
Crow, J. & Kimura, M. An Introduction To Population Genetics Theory. (Alpha Editions, 1970).Prado-Martinez, J. et al. Great ape genetic diversity and population history. Nature 499, 471 (2013).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Digitale, J. C. et al. HLA alleles B* 53:01 and C* 06:02 are associated with higher risk of P. falciparum parasitemia in a cohort in Uganda. Front. Immunol. 12, 650028 (2021).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Lyke, K. E. et al. Association of HLA alleles with Plasmodium falciparum severity in Malian children. Tissue Antigens. 77, 562–571 (2011).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Osafo-Addo, A. D. et al. HLA-DRB1*04 allele is associated with severe malaria in northern Ghana. Am. J. Trop. Med. 78, 251–255 (2008).Article 

Google Scholar 
Jallow, M. et al. Genome-wide and fine-resolution association analysis of malaria in West Africa. Nat. Genet. 41, 657–665 (2009).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Malaria Genomic Epidemiology Network. Insights into malaria susceptibility using genome-wide data on 17,000 individuals from Africa, Asia and Oceania. Nat. Commun. 10, 5732 (2019).Article 
ADS 
CAS 

Google Scholar 
Ravenhall, M. et al. Novel genetic polymorphisms associated with severe malaria and under selective pressure in North-eastern Tanzania. PLoS Genet. 14, e1007172 (2018).Article 
PubMed 
PubMed Central 

Google Scholar 
Damena, D., Denis, A., Golassa, L. & Chimusa, E. R. Genome-wide association studies of severe P. falciparum malaria susceptibility: progress, pitfalls and prospects. BMC Med. Genom. 12, 1–14 (2019).Article 
CAS 

Google Scholar 
Kennedy, A. E., Ozbek, U. & Dorak, M. T. What has GWAS done for HLA and disease associations? Int. J. Immunogenet. 44, 195–211 (2017).Article 
CAS 
PubMed 

Google Scholar 
Tukwasibwe, S. et al. Variations in killer-cell immunoglobulin-like receptor and human leukocyte antigen genes and immunity to malaria. Cell. Mol. Immunol. 17, 799–806 (2020).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Leffler, E. M. et al. Multiple instances of ancient balancing selection shared between humans and chimpanzees. Science 339, 1578–1582 (2013).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Phillips, M. et al. Malaria. Nat. Rev. Dis. Prim. 3, 17050 (2017).Article 
PubMed 

Google Scholar 
Samandary, S. et al. Associations of HLA-A, HLA-B and HLA-C alleles frequency with prevalence of herpes simplex virus infections and diseases across global populations: implication for the development of an universal CD8+ T-cell epitope-based vaccine. Hum. Immunol. 75, 715–729 (2014).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Miranda-Katz, M. et al. Novel HLA-B7-restricted human metapneumovirus epitopes enhance viral clearance in mice and are recognized by human CD8+ T cells. Sci. Rep. 11, 20769 (2021).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Appanna, R., Ponnampalavanar, S., Lum Chai See, L. & Sekaran, S. D. Susceptible and protective HLA class 1 alleles against dengue fever and dengue hemorrhagic fever patients in a Malaysian population. PloS One 5, e13029 (2010).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
Gao, X. et al. Effect of a single amino acid change in MHC class I molecules on the rate of progression to AIDS. NEJM 344, 1668–1675 (2001).Article 
CAS 
PubMed 

Google Scholar 
Sharp, P. M. & Hahn, B. H. Origins of HIV and the AIDS pandemic. Cold Spring Harb. Perspect. Med. 1, a006841 (2011).Article 
PubMed 
PubMed Central 

Google Scholar 
Barbian, H. J. et al. CHIIMP: An automated high‐throughput microsatellite genotyping platform reveals greater allelic diversity in wild chimpanzees. Ecol. Evol. 8, 7946–7963 (2018).Article 
PubMed 
PubMed Central 

Google Scholar 
Sullivan, K. M., Mannucci, A., Kimpton, C. P. & Gill, P. A rapid and quantitative DNA sex test: fluorescence-based PCR analysis of X-Y homologous gene amelogenin. Biotechniques 15, 636–638 (1993). 640-631.CAS 
PubMed 

Google Scholar 
de Groot, N. G. et al. Nomenclature report 2019: major histocompatibility complex genes and alleles of Great and Small Ape and Old and New World monkey species. Immunogenet 72, 25–36 (2020).Article 

Google Scholar 
Zhang, J., Kobert, K., Flouri, T. & Stamatakis, A. PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 30, 614–620 (2014).Article 
CAS 
PubMed 

Google Scholar 
Thomsen, M., Lundegaard, C., Buus, S., Lund, O. & Nielsen, M. MHCcluster, a method for functional clustering of MHC molecules. Immunogenet 65, 655–665 (2013).Article 
CAS 

Google Scholar 
Maibach, V. & Vigilant, L. Reduced bonobo MHC class I diversity predicts a reduced viral peptide binding ability compared to chimpanzees. BMC Evol. Biol. 19, 1–15 (2019).Article 

Google Scholar 
Wroblewski, E. E., Parham, P. & Guethlein, L. A. Two to tango: co-evolution of hominid natural killer cell receptors and MHC. Front. Immunol. 10 https://doi.org/10.3389/fimmu.2019.00177 (2019).Raymond, M. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86, 248–249 (1995).Article 

Google Scholar 
Rousset, F. GENEPOP’007: a complete re‐implementation of the GENEPOP software for Windows and Linux. Mol. Ecol. Resour. 8, 103–106 (2008).Article 
PubMed 

Google Scholar 
Wilson, M. L. et al. Lethal aggression in Pan is better explained by adaptive strategies than human impacts. Nature 513, 414–417 (2014).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Cheng, L., Samuni, L., Lucchesi, S., Deschner, T. & Surbeck, M. Love thy neighbour: behavioural and endocrine correlates of male strategies during intergroup encounters in bonobos. Anim. Behav. 187, 319–330 (2022).Article 

Google Scholar 
Lucchesi, S. et al. Beyond the group: how food, mates, and group size influence intergroup encounters in wild bonobos. Behav. Ecol. 31, 519–532 (2020).Article 

Google Scholar 
Plumptre, A., Robbins, M. M. & Williamson, E. A. Gorilla beringei. The IUCN Red List of Threatened Species 2019: e.T39994A115576640. (2019).Maisels, F., Bergl, R. A. & Williamson, E. A. Gorilla gorilla (amended version of 2016 assessment). The IUCN Red List of Threatened Species 2018: e.T9404A136250858. (2018).Humle, T., Maisels, F., Oates, J.F., Plumptre, A. & Williamson, E.A. Pan troglodytes (errata version published in 2018). The IUCN Red List of Threatened Species 2016: e.T15933A129038584. (2016).Fruth, B. et al. Pan paniscus (errata version published in 2016). The IUCN Red List of Threatened Species 2016: e.T15932A102331567. (2016). More

Zala, S. M., Potts, W. K. & Penn, D. J. Scent-marking displays provide honest signals of health and infection. Behav. Ecol. 15, 338–344 (2004).Article 

Google Scholar 
Allen, M. L., Wallace, C. F. & Wilmers, C. C. Patterns in bobcat (Lynx rufus) scent marking and communication behaviors. J. Ethol. 33, 9–14 (2014).Article 

Google Scholar 
White, A. M., Swaisgood, R. R. & Zhang, H. The highs and lows of chemical communication in giant pandas (Ailuropoda melanoleuca): Effect of scent deposition height on signal discrimination. Behav. Ecol. Sociobiol. 51, 519–529 (2002).Article 

Google Scholar 
Scordato, E. S., Dubay, G. & Drea, C. M. Chemical composition of scent marks in the ringtailed lemur (Lemur catta): Glandular differences, seasonal variation, and individual signatures. Chem. Senses 32, 493–504 (2007).Article 
CAS 
PubMed 

Google Scholar 
Maynard Smith, J. & Harper, D. Animal Signals (Oxford University Press, 2003).
Google Scholar 
Stockley, P., Bottell, L. & Hurst, J. L. Wake up and smell the conflict: Odour signals in female competition. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 368, 20130082 https://doi.org/10.1098/rstb.2013.0082 (2013).Article 
PubMed 
PubMed Central 

Google Scholar 
Petrulis, A. Chemosignals, hormones and mammalian reproduction. Horm. Behav. 63, 723–741 (2013).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Coombes, H. A., Stockley, P. & Hurst, J. L. Female chemical signalling underlying reproduction in mammals. J. Chem. Ecol. 44, 851–873 (2018).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Harmsen, B. J., Foster, R. J., Gutierrez, S. M., Marin, S. Y. & Patrick, C. Scrape-marking behavior of jaguars (Panthera onca) and pumas (Puma concolor). J. Mammal. 91, 1225–1234 (2010).Article 

Google Scholar 
Lamb, C. T. et al. Density-dependent signaling: An alternative hypothesis on the function of chemical signaling in a non-territorial solitary carnivore. PLoS ONE 12, e0184176 https://doi.org/10.1371/journal.pone.0184176 (2017).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Woodmansee, K. B., Zabel, C. J., Glickman, S. E., Frank, L. G. & Keppel, G. Scent marking (pasting) in a colony of immature spotted hyenas (Crocuta crocuta): A developmental study. J. Comp. Psychol. 105, 10–14 (1991).Article 
CAS 
PubMed 

Google Scholar 
Rasmussen, L. E. L., Riddle, H. S. & Krishnamurthy, V. Mellifluous matures to malodorous in musth. Nature 415, 975–976 (2002).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Surov, A. V. & Maltsev, A. N. Analysis of chemical communication in mammals: Zoological and ecological aspects. Biol. Bull. 43, 1175–1183 (2016).Article 

Google Scholar 
Hurst, J. L. Female recognition and assessment of males through scent. Behav. Brain Res. 200, 295–303 (2009).Article 
CAS 
PubMed 

Google Scholar 
Mills, M. G. L. & Gorman, M. L. The scent-marking behaviour of the spotted hyaena Crocuta crocuta in the southern Kalahari. J. Zool. 212, 483–497 (1987).Article 

Google Scholar 
Gassett, J. W. et al. Volatile compounds from interdigital gland of male white-tailed deer (Odocoileus virginianus). J. Chem. Ecol. 22, 1689–1696 (1996).Article 
CAS 
PubMed 

Google Scholar 
Stoeckelhuber, M., Sliwa, A. & Welsch, U. Histo-physiology of the scent-marking glands of the penile pad, anal Pouch, and the forefoot in the aardwolf (Proteles cristatus). Anat. Rec. 259, 312–326 (2000).Article 
CAS 

Google Scholar 
Begg, C. M., Begg, K. S., Du Toit, J. T. & Mills, M. G. L. Scent-marking behaviour of the honey badger, Mellivora capensis (Mustelidae), in the southern Kalahari. Anim. Behav. 66, 917–929 (2003).Article 

Google Scholar 
Yasui, T., Tsukise, A. & Meyer, W. Histochemical analysis of glycoconjugates in the eccrine glands of the raccoon digital pads. Eur. J. Histochem. 48, 393–402 (2004).CAS 
PubMed 

Google Scholar 
Johnston, R. E. Scent marking by male golden hamsters (Mesocricetus aurutus) I. Effects of odors and social encounters. Z. Tierpsychol. 37, 75–98 (1975).Article 
CAS 
PubMed 

Google Scholar 
Caspers, B., Wibbelt, G. & Voigt, C. C. Histological examinations of facial glands in Saccopteryx bilineata (Chiroptera, Emballonuridae), and their potential use in territorial marking. Zoomorphology 128, 37–43 (2008).Article 

Google Scholar 
Lawson, R. E., Putnam, R. J. & Fielding, A. H. Individual signatures in scent gland secretions of Eurasian deer. J. Zool. 251, 399–410 (2000).Article 

Google Scholar 
Smith, T. E., Tomlinson, A. J., Mlotkiewicz, J. A. & Abbott, D. H. Female marmoset monkeys (Callithrix jacchus) can be identified from the chemical composition of their scent marks. Chem. Senses 26, 449–458 (2001).Article 
CAS 
PubMed 

Google Scholar 
del Barco-Trillo, J., LaVenture, A. B. & Johnston, R. E. Male hamsters discriminate estrous state from vaginal secretions and individuals from flank marks. Behav. Process. 82, 18–24 (2009).Article 

Google Scholar 
Sun, L. & Müller-Schwarze, D. Anal gland secretion codes for family membership in the beaver. Behav. Ecol. Sociobiol. 44, 199–208 (1998).Article 

Google Scholar 
Zhang, J. X. et al. Possible coding for recognition of sexes, individuals and species in anal gland volatiles of Mustela eversmanni and M. sibirica. Chem. Senses 28, 381–388 (2003).Article 
PubMed 

Google Scholar 
Kean, E. F., Müller, C. T. & Chadwick, E. A. Otter scent signals age, sex, and reproductive status. Chem. Senses 36, 555–564 (2011).Article 
CAS 
PubMed 

Google Scholar 
Rosell, F. et al. Brown bears possess anal sacs and secretions may code for sex. J. Zool. 283, 143–152 (2011).Article 

Google Scholar 
Buesching, C. D., Waterhouse, J. S. & Macdonald, D. W. Gas-chromatographic analyses of the subcaudal gland secretion of the European badger (Meles meles) part I: Chemical differences related to individual parameters. J. Chem. Ecol. 28, 41–56 (2002).Article 
CAS 
PubMed 

Google Scholar 
Yuan, H. et al. Anogenital gland secretions code for sex and age in the giant panda, Ailuropoda melanoleuca. Can. J. Zool. 82, 1596–1604 (2004).Article 

Google Scholar 
Kent, L. & Tang-Martínez, Z. Evidence of individual odors and individual discrimination in the raccoon, Procyon lotor. J. Mammal. 95, 1254–1262 (2014).Article 

Google Scholar 
Woodley, S. K. & Baum, M. J. Differential activation of glomeruli in the ferret’s main olfactory bulb by anal scent gland odours from males and females: An early step in mate identification. Eur. J. Neurosci. 20, 1025–1032 (2004).Article 
PubMed 
PubMed Central 

Google Scholar 
Allen, M. L. et al. The role of scent marking in mate selection by female pumas (Puma concolor). PLoS ONE 10, e0139087 https://doi.org/10.1371/journal.pone.0139087 (2015).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Latour, P. Interactions between free-ranging, adult male polar bears (Ursus maritimus Phipps): A case of adult social play. Can. J. Zool. 59, 1775–1783 (1981).Article 

Google Scholar 
Nie, Y., Swaisgood, R. R., Zhang, Z., Liu, X. & Wei, F. Reproductive competition and fecal testosterone in wild male giant pandas (Ailuropoda melanoleuca). Behav. Ecol. Sociobiol. 66, 721–730 (2012).Article 

Google Scholar 
Clapham, M. & Kitchin, J. Social play in wild brown bears of varying age-sex class. Acta Ethol. 19, 181–188 (2016).Article 

Google Scholar 
Stonorov, D. & Stokes, A. W. Social behavior of the Alaska brown bear. Int. Conf. Bear Res. Manag. 2, 232–242 (1972).
Google Scholar 
Clapham, M., Nevin, O. T., Ramsey, A. D. & Rosell, F. A hypothetico-deductive approach to assessing the social function of chemical signalling in a non-territorial solitary carnivore. PLoS ONE 7, e35404 https://doi.org/10.1371/journal.pone.0035404 (2012).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Clapham, M., Nevin, O. T., Ramsey, A. D. & Rosell, F. The function of strategic tree selectivity in the chemical signalling of brown bears. Anim. Behav. 85, 1351–1357 (2013).Article 

Google Scholar 
Owen, M. A. et al. An experimental investigation of chemical communication in the polar bear. J. Zool. 295, 36–43 (2015).Article 

Google Scholar 
Sergiel, A. et al. Histological, chemical and behavioural evidence of pedal communication in brown bears. Sci. Rep. 7, 1052 https://doi.org/10.1038/s41598-017-01136-1 (2017).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Tomiyasu, J. et al. Morphological and histological features of the vomeronasal organ in the brown bear. J. Anat. 231, 749–757 (2017).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Tomiyasu, J. et al. Testicular regulation of seasonal change in apocrine glands in the back skin of the brown bear (Ursus arctos). J. Vet. Med. Sci. 80, 1034–1040 (2018).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Tomiyasu, J. et al. Testosterone-related and seasonal changes in sebaceous glands in the back skin of adult male brown bears (Ursus arctos). Can. J. Zool. 96, 205–211 (2018).Article 
CAS 

Google Scholar 
Burst, T. L. & Pelton, M. R. Black bear mark trees in the Smoky mountains. Int. Conf. Bear Res. Manag. 5, 45–53 (1983).
Google Scholar 
Mattson, D. J. & Greene, G. I. Tree rubbing by Yellowstone grizzly bears Ursus arctos. Wildl. Biol. 1, 1–9 (2003).
Google Scholar 
Nie, Y. et al. Giant panda scent-marking strategies in the wild: Role of season, sex and marking surface. Anim. Behav. 84, 39–44 (2012).Article 

Google Scholar 
Revilla, E. et al. Brown bear communication hubs: Patterns and correlates of tree rubbing and pedal marking at a long-term marking site. PeerJ 9, 10447 https://doi.org/10.7717/peerj.10447 (2021).Article 

Google Scholar 
Clapham, M., Nevin, O. T., Ramsey, A. D. & Rosell, F. Scent-marking investment and motor patterns are affected by the age and sex of wild brown bears. Anim. Behav. 94, 107–116 (2014).Article 

Google Scholar 
Taylor, A. P., Gunther, M. S. & Allen, M. L. Black bear marking behaviour at rub trees during the breeding season in northern California. Behaviour 152, 1097–1111 (2015).Article 

Google Scholar 
Filipczyková, E., Heitkönig, I., Castellanos, A., Hantson, W. & Steyaert, S. Marking behavior of Andean bears in an Ecuadorian cloud forest: A pilot study. Ursus 27, 122–128 (2017).Article 

Google Scholar 
Stringham, S. F. Aggressive body language of bears and wildlife viewing: A response to Geist (2011). Hum.-Wildl. Interact. 5, 4 (2011).
Google Scholar 
Swaisgood, R. R., Lindburg, D. G. & Zhang, H. Discrimination of oestrous status in giant pandas (Ailuropoda melanoleuca) via chemical cues in urine. J. Zool. 257, 381–386 (2002).Article 

Google Scholar 
Wilson, A. E. et al. Behavioral, semiochemical and androgen responses by male giant pandas to the olfactory sexual receptivity cues of females. Theriogenology 114, 330–337 (2018).Article 
CAS 
PubMed 

Google Scholar 
Sillero-Zubiri, C. & Macdonald, D. W. Scent-marking and territorial behaviour of Ethiopian wolves Canis simensis. J. Zool. 245, 351–361 (1998).Article 

Google Scholar 
Stępniak, K. M., Niedźwiecka, N., Szewczyk, M. & Mysłajek, R. W. Scent marking in wolves Canis lupus inhabiting managed lowland forests in Poland. Mammal Res. 65, 629–638 (2020).Article 

Google Scholar 
Liu, D. et al. Do anogenital gland secretions of giant panda code for their sexual ability? Chin. Sci. Bull. 51, 1986–1995 (2006).Article 
CAS 

Google Scholar 
Tattoni, C., Bragalanti, N., Groff, C. & Rovero, F. Patterns in the use of rub trees by the Eurasian brown bear. Hystrix 26, 118 (2015).
Google Scholar 
Zhang, J. X. et al. Potential chemosignals in the anogenital gland secretion of giant pandas, Ailuropoda melanoleuca, associated with sex and individual identity. J. Chem. Ecol. 34, 398–407 (2008).Article 
CAS 
PubMed 

Google Scholar 
Swaisgood, R. R., Lindburg, D. G., Zhou, X. & Owen, M. A. The effects of sex, reproductive condition and context on discrimination of conspecific odours by giant pandas. Anim. Behav. 60, 227–237 (2000).Article 
CAS 
PubMed 

Google Scholar 
Swaisgood, R., Lindburg, D. & Zhou, X. Giant pandas discriminate individual differences in conspecific scent. Anim. Behav. 57, 1045–1053 (1999).Article 
CAS 
PubMed 

Google Scholar 
Liu, D. et al. Do urinary chemosignals code for sex, age, and season in the giant panda, Ailuropoda melanoleuca? in Chemical Signals in Vertebrates. Vol. 12. 207–222 (eds. East, M. L. & Dehnhard, M.). https://doi.org/10.1007/978-1-4614-5927-9_16 (Springer, 2013).Hagey, L. & MacDonald, E. Chemical cues identify gender and individuality in giant pandas (Ailuropoda melanoleuca). J. Chem. Ecol. 29, 1479–1488 (2003).Article 
CAS 
PubMed 

Google Scholar 
Wilson, A. E., Sparks, D. L., Knott, K. K., Willard, S. & Brown, A. Implementing solid phase microextraction (SPME) as a tool to detect volatile compounds produced by giant pandas in the environment. PLoS ONE 13, e0208618 https://doi.org/10.1371/journal.pone.0208618 (2018).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Wilson, A. E. et al. Field air analysis of volatile compounds from free-ranging giant pandas. Ursus 29, 75–81 (2019).Article 

Google Scholar 
Crupi, A. P., Waite, J. N., Flynn, R. W. & Beier, L. Brown bear population estimation in Yakutat, Southeast Alaska. Alaska Department of Fish and Game https://doi.org/10.13140/RG.2.2.35947.54568 (2017).Article 

Google Scholar 
Sikes, R. S., Gannon, W. L. & The Animal Care and Use Committee of the American Society of Mammalogists. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J. Mammal. 92, 235–253 (2011).Matson, G. et al. A Laboratory Manual for Cementum Age Determination of Alaska Brown Bear First Premolar Teeth. Alaska Department of Fish and Game, Division of Wildlife Conservation https://www.adfg.alaska.gov/index.cfm?adfg=librarypublications.wildlifepublicationsdetails&pubidentifier=3374 (1993).Seryodkin, I. V. Marking activity of the Kamchatka brown bear (Ursus arctos piscator). Achiev. Life Sci. 8, 153–161 (2014).
Google Scholar 
Peralbo-Molina, A., Calderón-Santiago, M., Jurado-Gámez, B., Luque De Castro, M. D. & Priego-Capote, F. Exhaled breath condensate to discriminate individuals with different smoking habits by GC-TOF/MS. Sci. Rep. 7, 1421 https://doi.org/10.1038/s41598-017-01564-z (2017).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Liu, D. et al. Male panda (Ailuropoda melanoleuca) urine contains kinship information. Chin. Sci. Bull. 53, 2793–2800 (2008).CAS 

Google Scholar 
Kean, E. F., Chadwick, E. A. & Müller, C. T. Scent signals individual identity and country of origin in otters. Mamm. Biol. Z. Säugetierkd. 80, 99–105 (2015).Article 

Google Scholar 
R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.r-project.org/ (2020).Harris, R. L., Holland, B. R., Cameron, E. Z., Davies, N. W. & Nicol, S. C. Chemical signals in the echidna: Differences between seasons, sexes, individuals and gland types. J. Zool. 293, 171–180 (2014).Article 

Google Scholar 
Vaglio, S. et al. Sternal gland scent-marking signals sex, age, rank, and group identity in captive mandrills. Chem. Senses 41, 177–186 (2016).PubMed 

Google Scholar 
Knott, K. K. et al. Blood-based biomarkers of selenium and thyroid status indicate possible adverse biological effects of mercury and polychlorinated biphenyls in Southern Beaufort Sea polar bears. Environ. Res. 111, 1124–1136 (2011).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Wilson, A. E. et al. Development and validation of protein biomarkers of health in grizzly bears. Conserv. Physiol. 8, coaa056 https://doi.org/10.1093/conphys/coaa056 (2020).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Oksanen, J. et al. Vegan: community ecology package. R package version 2.6-4. https://CRAN.R-project.org/package=vegan (2020).Williams, C. L., Ybarra, A. R., Meredith, A. N., Durrant, B. S. & Tubbs, C. W. Gut microbiota and phytoestrogen-associated infertility in Southern White Rhinoceros. MBio 10, e00311-19 https://doi.org/10.1128/mBio.00311-19 (2019).Article 
PubMed 
PubMed Central 

Google Scholar 
Dill-McFarland, K. A., Breaker, J. D. & Suen, G. Microbial succession in the gastrointestinal tract of dairy cows from 2 weeks to first lactation. Sci. Rep. 7, 40864 https://doi.org/10.1038/srep40864 (2017).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Williams, C. L. et al. Dietary changes during weaning shape the gut microbiota of red pandas (Ailurus fulgens). Conserv. Physiol. 6, cox075 https://doi.org/10.1093/conphys/cox075 (2018).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Bolar, K. STAT: interactive document for working with basic statistical analysis. R package version 0.1.0. https://CRAN.R-project.org/package=STAT (2019).Gese, E. & Ruff, R. Scent-marking by coyotes, Canis latrans: The influence of social and ecological factors. Anim. Behav. 54, 1155–1166 (1997).Article 
CAS 
PubMed 

Google Scholar 
Thompson, C. L. et al. What smells? Developing in-field methods to characterize the chemical composition of wild mammalian scent cues. Ecol. Evol. 10, 4691–4701 (2020).Article 
PubMed 
PubMed Central 

Google Scholar 
Charpentier, M. J. E., Barthes, N., Proffit, M., Bessière, J.-M. & Grison, C. Critical thinking in the chemical ecology of mammalian communication: Roadmap for future studies. Funct. Ecol. 26, 769–774 (2012).Article 

Google Scholar 
Martín, J., Carranza, J., López, P., Alarcos, S. & Pérez-González, J. A new sexual signal in rutting male red deer: Age related chemical scent constituents in the belly black spot. Mamm. Biol. 79, 362–368 (2014).Article 

Google Scholar 
Carranza, J. et al. The dark ventral patch: A bimodal flexible trait related to male competition in red deer. PLoS ONE 15, 0241374 https://doi.org/10.1371/journal.pone.0241374 (2020).Article 
CAS 

Google Scholar 
Kean, E. F., Bruford, M. W., Russo, I. R. M., Müller, C. T. & Chadwick, E. A. Odour dialects among wild mammals. Sci. Rep. 7, 13593 https://doi.org/10.1038/s41598-017-12706-8 (2017).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Marneweck, C., Jürgens, A. & Shrader, A. M. The role of middens in white rhino olfactory communication. Anim. Behav. 140, 7–18 (2018).Article 

Google Scholar 
Linklater, W. L., Mayer, K. & Swaisgood, R. R. Chemical signals of age, sex and identity in black rhinoceros. Anim. Behav. 85, 671–677 (2013).Article 

Google Scholar 
White, A. M., Swaisgood, R. R. & Zhang, H. Chemical communication in the giant panda (Ailuropoda melanoleuca): The role of age in the signaller and assessor. J. Zool. 259, 171–178 (2003).Article 

Google Scholar 
Steiger, S., Schmitt, T. & Schaefer, H. M. The origin and dynamic evolution of chemical information transfer. Proc. R. Soc. B Biol. Sci. 278, 970–979 https://doi.org/10.1098/rspb.2010.2285 (2011).Article 

Google Scholar 
Williams, C. L. et al. Wildlife-microbiome interactions and disease: Exploring opportunities for disease mitigation across ecological scales. Drug Discov. Today Dis. Models 28, 105–115 (2018).Article 

Google Scholar 
Chiang, Y. R., Wei, S. T. S., Wang, P. H., Wu, P. H. & Yu, C. P. Microbial degradation of steroid sex hormones: Implications for environmental and ecological studies. Microb. Biotechnol. 13, 926–949 (2020).Article 
CAS 
PubMed 

Google Scholar 
Williams, C. L., Garcia-Reyero, N., Martyniuk, C. J., Tubbs, C. W. & Bisesi, J. H. Regulation of endocrine systems by the microbiome: Perspectives from comparative animal models. Gen. Comp. Endocrinol. 292, 113437 (2020).Article 
CAS 
PubMed 

Google Scholar 
Theis, K. R., Venkataraman, A., Wagner, A. P., Holekamp, K. E. & Schmidt, T. M. Age-related variation in the scent pouch bacterial communities of striped hyenas (Hyaena hyaena). Chem. Signals Vertebr. 13, 87–103 (2016).Article 

Google Scholar 
Steyaert, S. M. J. G., Endrestøl, A., Hackländer, K., Swenson, J. E. & Zedrosser, A. The mating system of the brown bear Ursus arctos. Mammal Rev. 42, 12–34 (2012).Article 

Google Scholar 
Bellemain, E. et al. The dilemma of female mate selection in the brown bear, a species with sexually selected infanticide. Proc. R. Soc. B Biol. Sci. 273, 283–291 https://doi.org/10.1098/rspb.2005.3331 (2006).Article 

Google Scholar 
Zedrosser, A., Bellemain, E., Taberlet, P. & Swenson, J. E. Genetic estimates of annual reproductive success in male brown bears: The effects of body size, age, internal relatedness and population density. J. Anim. Ecol. 76, 368–375 (2007).Article 
PubMed 

Google Scholar 
Schwartz, C. C. et al. Reproductive maturation and senescence in the female brown bear. Ursus 14, 109–119 (2003).
Google Scholar 
Schulte, B. A., Freeman, E. W., Goodwin, T. E., Hollister-Smith, J. & Rasmussen, L. E. L. Honest signalling through chemicals by elephants with applications for care and conservation. Appl. Anim. Behav. Sci. 102, 344–363 (2007).Article 

Google Scholar 
Støen, O.-G., Bellemain, E., Sæbø, S. & Swenson, J. E. Kin-related spatial structure in brown bears Ursus arctos. Behav. Ecol. Sociobiol. 59, 191–197 (2005).Article 

Google Scholar 
Egbert, A. L. & Stokes, A. W. The social behaviour of brown bears on an Alaskan salmon stream. Int. Conf. Bear Res. Manag. 3, 41–56 (1976).
Google Scholar 
Craighead, J. J., Sumner, J. S. & Mitchell, J. A. The Grizzly Bears of Yellowstone: Their Ecology in the Yellowstone Ecosystem, 1959–1992 (Island Press, 1995).
Google Scholar 
Burgener, N., Dehnhard, M., Hofer, H. & East, M. L. Does anal gland scent signal identity in the spotted hyaena? Anim.
Behav. 77, 707–715 (2009).Article 

Google Scholar 
Noonan, M. J. et al. Knowing me, knowing you: Anal gland secretion of European badgers (Meles meles) codes for individuality, sex and social group membership. J. Chem. Ecol. 45, 823–837 (2019).Article 
CAS 
PubMed 

Google Scholar 
Sun, L. & Müller-Schwarze, D. Sibling recognition in the beaver: A field test for phenotype matching. Anim. Behav. 54, 493–502 (1997).Article 
CAS 
PubMed 

Google Scholar 
Thom, M. D. & Hurst, J. L. Individual recognition by scent. Ann. Zool. Fenn. 41, 765–787 (2004).
Google Scholar 
Roberts, S. A. et al. Individual odour signatures that mice learn are shaped by involatile major urinary proteins (MUPs). BMC Biol. 16, 1–19 https://doi.org/10.1186/s12915-018-0512-9 (2018).Article 
CAS 

Google Scholar 
Henkel, S. & Setchell, J. M. Group and kin recognition via olfactory cues in chimpanzees (Pan troglodytes). Proc. R. Soc. B Biol. Sci. 285, 20181527 https://doi.org/10.1098/rspb.2018.1527 (2018).Article 

Google Scholar 
Vogt, K., Boos, S., Breitenmoser, U. & Kölliker, M. Chemical composition of Eurasian lynx urine conveys information on reproductive state, individual identity, and urine age. Chemoecology 26, 205–217 (2016).Article 
CAS 

Google Scholar 
Wyatt, T. D. Pheromones and signature mixtures: Defining species-wide signals and variable cues for identity in both invertebrates and vertebrates. J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 196, 685–700 (2010).Article 
CAS 
PubMed 

Google Scholar 
Johnston, R. E. Chemical communication in rodents: From pheromones to individual recognition. J. Mammal. 84, 1141–1162 (2003).Article 

Google Scholar 
Dehnhard, M. Mammal semiochemicals: Understanding pheromones and signature mixtures for better zoo-animal husbandry and conservation. Int. Zoo Yearb. 45, 55–79 (2011).Article 

Google Scholar 
Brennan, P. A. & Kendrick, K. M. Mammalian social odours: Attraction and individual recognition. Philos. Trans. R. Soc. B Biol. Sci. 361, 2061–2078 https://doi.org/10.1098/rstb.2006.1931 (2006).Article 
CAS 

Google Scholar 
Bellemain, E., Swenson, J. E. & Taberlet, P. Mating strategies in relation to sexually selected infanticide in a non-social carnivore: The brown bear. Ethology 112, 238–246 (2006).Article 

Google Scholar 
Rogers, L. L. Effects of food supply and kinship on social behavior, movements, and population growth of black bears in northeastern Minnesota. Wildl. Monogr. 97, 72 (1987).
Google Scholar 
Noyce, K. V. & Garshelis, D. L. Follow the leader: Social cues help guide landscape-level movements of American black bears (Ursus americanus). Can. J. Zool. 92, 1005–1017 (2014).Article 

Google Scholar 
Hansen, J. E., Hertel, A. G., Frank, S. C., Kindberg, J. & Zedrosser, A. Social environment shapes female settlement decisions in a solitary carnivore. Behav. Ecol. 33, 137–146 (2022).Article 
CAS 
PubMed 

Google Scholar 
Morehouse, A. T., Loosen, A. E., Graves, T. A. & Boyce, M. S. The smell of success: Reproductive success related to rub behavior in brown bears. PLoS ONE 16, 247964 https://doi.org/10.1371/journal.pone.0247964 (2021).Article 
CAS 

Google Scholar 
Tschanz, B., Meyer-Holzapfel, M. & Bachmann, S. Das informationssystem bei Braunbären. Z. Tierpsychol. 27, 47–72 (1970).Article 

Google Scholar 
Tattoni, C., Bragalanti, N., Ciolli, M., Groff, C. & Rovero, F. Behavior of the European brown bear at rub trees. Ursus 32e9, 1–11https://doi.org/10.2192/URSUS-D-20-00022.3 (2021).Article 

Google Scholar 
Alberts, A. C. Constraints on the design of chemical communication systems in terrestrial vertebrates. Am. Nat. 139, S62–S89 (1992).Article 

Google Scholar  More

Whittaker, R. J., Fernández-Palacios, J. M., Matthews, T. J., Borregaard, M. K. & Triantis, K. A. Island biogeography: taking the long view of nature’s laboratories. Science 357, eaam8326 (2017).Article 
PubMed 

Google Scholar 
Boyer, A. G. & Jetz, W. Biogeography of body size in Pacific island birds. Ecography 33, 369–379 (2010).
Google Scholar 
Heinen, J. H., van Loon, E. E., Hansen, D. M. & Kissling, W. D. Extinction‐driven changes in frugivore communities on oceanic islands. Ecography 41, 1245–1255 (2018).Article 

Google Scholar 
Sayol, F., Steinbauer, M. J., Blackburn, T. M., Antonelli, A. & Faurby, S. Anthropogenic extinctions conceal widespread evolution of flightlessness in birds. Sci. Adv. 6, eabb6095 (2020).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
Steadman, D. W. & Martin, P. S. The late quaternary extinction and future resurrection of birds on Pacific islands. Earth Sci. Rev. 61, 133–147 (2003).Article 
ADS 

Google Scholar 
Blackburn, T. M., Cassey, P., Duncan, R. P., Evans, K. L. & Gaston, K. J. Avian extinction and mammalian introductions on oceanic islands. Science 305, 1955–1958 (2004).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Blackburn, T. M., Lockwood, J. L., & Cassey, P. (2009). Avian Invasions: The Ecology and Evolution of Exotic Birds (Oxford University Press, 2009).Steadman, D. W. Extinction and Biogeography of Tropical Pacific Birds (University of Chicago Press, 2006).Boyer, A. G. & Jetz, W. Extinctions and the loss of ecological function in island bird communities. Glob. Ecol. Biogeogr. 23, 679–688 (2014).Article 

Google Scholar 
Fritts, T. H. & Rodda, G. H. The role of introduced species in the degradation of island ecosystems: a case history of Guam. Annu. Rev. Ecol. Syst. 29, 113–140 (1998).Article 

Google Scholar 
Vidal, M. M. et al. Frugivores at higher risk of extinction are the key elements of a mutualistic network. Ecology 95, 3440–3447 (2014).Article 

Google Scholar 
Pires, M. M. et al. Reconstructing past ecological networks: the reconfiguration of seed-dispersal interactions after megafaunal extinction. Oecologia 175, 1247–1256 (2014).Article 
ADS 
PubMed 

Google Scholar 
Heinen, J. H., Rahbek, C. & Borregaard, M. K. Conservation of species interactions to achieve self-sustaining ecosystems. Ecography 43, 1603–1611 (2020).Article 

Google Scholar 
Moreno-Mateos, D. et al. The long-term restoration of ecosystem complexity. Nat. Ecol. Evol. 4, 676–685 (2020).Article 
PubMed 

Google Scholar 
Galetti, M. et al. Functional extinction of birds drives rapid evolutionary changes in seed size. Science 340, 1086–1090 (2013).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Dunn, R. R. Coextinction: anecdotes, models, and speculation. In Holocene Extinctions (ed. Turvey, S. T.) 167–180 (Oxford University Press, 2009).Rezende, E. L., Lavabre, J. E., Guimarães, P. R., Jordano, P. & Bascompte, J. Non-random coextinctions in phylogenetically structured mutualistic networks. Nature 448, 925–928 (2007).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Wotton, D. M. & Kelly, D. Do larger frugivores move seeds further? Body size, seed dispersal distance, and a case study of a large, sedentary pigeon. J. Biogeogr. 39, 1973–1983 (2012).Article 

Google Scholar 
Anderson, S. H., Kelly, D., Ladley, J. J., Molloy, S. & Terry, J. Cascading effects of bird functional extinction reduce pollination and plant density. Science 331, 1068–1071 (2011).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Pérez-Méndez, N., Jordano, P., García, C. & Valido, A. The signatures of Anthropocene defaunation: cascading effects of the seed dispersal collapse. Sci. Rep. 6, 1–9 (2016).Article 

Google Scholar 
Wotton, D. M. & Kelly, D. Frugivore loss limits recruitment of large-seeded trees. Proc. R. Soc. B Biol. Sci. 278, 3345–3354 (2011).Article 

Google Scholar 
Traveset, A. Effect of seed passage through vertebrate frugivores’ guts on germination: a review. Perspect. Plant Ecol. Evol. Syst. 1, 151–190 (1998).Article 

Google Scholar 
Janzen, D. H. Herbivores and the number of tree species in tropical forests. Am. Nat. 104, 501–528 (1970).Article 

Google Scholar 
Connell, J. H. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In Dynamics of Populations (eds Den Boer, P. J. & Gradwell, G. R.) 298–312 (Centre for Agricultural Publishing and Documentation, 1971).Farwig, N. & Berens, D. G. Imagine a world without seed dispersers: a review of threats, consequences and future directions. Basic Appl. Ecol. 13, 109–115 (2012).Article 

Google Scholar 
Meehan, H. J., McConkey, K. R. & Drake, D. R. Potential disruptions to seed dispersal mutualisms in Tonga, Western Polynesia. J. Biogeogr. 29, 695–712 (2002).Article 

Google Scholar 
Pérez-Méndez, N., Jordano, P. & Valido, A. Downsized mutualisms: consequences of seed dispersers’ body-size reduction for early plant recruitment. Perspect. Plant Ecol. Evol. Syst. 17, 151–159 (2015).Article 

Google Scholar 
Rodriguez, L. F. Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biol. Invasions 8, 927–939 (2006).Article 

Google Scholar 
Griffiths, C. J., Hansen, D. M., Jones, C. G., Zuël, N. & Harris, S. Resurrecting extinct interactions with extant substitutes. Curr. Biol. 21, 762–765 (2011).Article 
CAS 
PubMed 

Google Scholar 
Thibault, J.-C. & Cibois, A. Birds Of Eastern Polynesia: A Biogeographic Atlas (Lynx Edicions, 2017).Vizentin-Bugoni, J. et al. Structure, spatial dynamics, and stability of novel seed dispersal mutualistic networks in Hawaiʻi. Science 364, 78–82 (2019).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Case, S. B. & Tarwater, C. E. Functional traits of avian frugivores have shifted following species extinction and introduction in the Hawaiian Islands. Funct. Ecol. 34, 2467–2476 (2020).Article 

Google Scholar 
Albert, S., Flores, O. & Strasberg, D. Collapse of dispersal trait diversity across a long‐term chronosequence reveals a strong negative impact of frugivore extinctions on forest resilience. J. Ecol. 108, 1386–1397 (2020).Article 

Google Scholar 
Cheke, A. S. & Hume, J. P. Lost Land of the Dodo: The Ecological History of Mauritius, Réunion & Rodrigues 464 (T. & A. D. Poyser, 2008).Hammond, D. S. et al. Threats to environmentally sensitive areas from peri-urban expansion in Mauritius. Environ. Conserv. 42, 256–267 (2015).Article 

Google Scholar 
Florens, F. V., Baider, C., Seegoolam, N. B., Zmanay, Z. & Strasberg, D. Long‐term declines of native trees in an oceanic island’s tropical forests invaded by alien plants. Appl. Veg. Sci. 20, 94–105 (2017b).Article 

Google Scholar 
McConkey, K. R. & O’Farrill, G. Cryptic function loss in animal populations. Trends Ecol. Evol. 30, 182–189 (2015).Article 
PubMed 

Google Scholar 
Carpenter, J. K. et al. The forgotten fauna: Native vertebrate seed predators on islands. Funct. Ecol. 34, 1802–1813 (2020).Article 

Google Scholar 
Perea, R., Delibes, M., Polko, M., Suárez-Esteban, A. & Fedriani, J. M. Context‐dependent fruit–frugivore interactions: partner identities and spatio‐temporal variations. Oikos 122, 943–951 (2013).Article 

Google Scholar 
Dracxler, C. M. & Kissling, W. D. The mutualism–antagonism continuum in Neotropical palm–frugivore interactions: from interaction outcomes to ecosystem dynamics. Biol. Rev. 97, 527–553 (2022).Article 

Google Scholar 
Baider, C. & Florens, F. B. V. Current decline of the ‘Dodo-tree’: a case of broken-down interactions with extinct species or the result of new interactions with alien invaders? In Emerging Threats to Tropical Forests (eds Laurance, W. & Peres, C.) 199–214 (Chicago University Press, 2006).Reinegger, R. D., Oleksy, R. Z., Bissessur, P., Naujeer, H. & Jones, G. First come, first served: fruit availability to keystone bat species is potentially reduced by invasive macaques. J. Mammal. 102, 428–439 (2021).Article 

Google Scholar 
Reinegger, R. D., Oleksy, R. Z., Gazagne, E. & Jones, G. Foraging strategies of invasive Macaca fascicularis may promote plant invasion in Mauritius. Int. J. Primatol. 44, 1–31 (2022).O’Connor, S. J. & Kelly, D. Seed dispersal of matai (Prumnopitys taxifolia) by feral pigs (Sus scrofa). N.Z. J. Ecol. 36, 228–231 (2012).
Google Scholar 
Shiels, A. B. & Drake, D. R. Are introduced rats (Rattus rattus) both seed predators and dispersers in Hawaii? Biol. Invasions 13, 883–894 (2011).Article 

Google Scholar 
Florens, F. B. V. et al. Disproportionately large ecological role of a recently mass-culled flying fox in native forests of an oceanic island. J. Nat. Conserv. 40, 85–93 (2017a).Article 

Google Scholar 
Bissessur, P., Bunsy, Y., Baider, C. & Florens, F. B. V. Non-intrusive systematic study reveals mutualistic interactions between threatened island endemic species and points to more impactful conservation. J. Nat. Conserv. 49, 108–117 (2019).Article 

Google Scholar 
Hume, J. P. & Winters, R. Captive birds on Dutch Mauritius: bad-tempered parrots, warty pigeons and notes on other native animals. Hist. Biol. 28, 812–822 (2016).Article 

Google Scholar 
Kingston, T., Florens, F. B. V., Oleksy, R., Ruhomaun, K. & Tatayah, V. Pteropus niger. The IUCN Red List of Threatened Species (2018).Hume, J. P. The history of the dodo Raphus cucullatus and the penguin of Mauritius. Hist. Biol. 18, 65–89 (2006).Article 

Google Scholar 
Hume, J. P. Reappraisal of the parrots (Aves: Psittacidae) from the Mascarene Islands, with comments on their ecology, morphology and affinities. Zootaxa 1513, 1–76 (2007).Article 

Google Scholar 
Hume, J. P. Systematics, morphology, and ecological history of the Mascarene starlings (Aves: Sturnidae) with the description of a new genus and species from Mauritius. Zootaxa 3849, 1–75 (2014).Article 
PubMed 

Google Scholar 
Albert, S., Flores, O., Baider, C., Florens, F. B. V. & Strasberg, D. Differing severity of frugivore loss contrasts the fate of native forests on the land of the Dodo (Mascarene archipelago). Biol. Conserv. 257, 109–131 (2021).Article 

Google Scholar 
Florens, F. B. V. Conservation in Mauritius and Rodrigues: challenges and achievements from two ecologically devastated oceanic islands. In Conservation Biology: Voices from the Tropics (eds Raven, P. H., Sodhi, N. S. & Gibson, L.) 40–50 (Wiley-Blackwell, 2013).Krivek, G., Florens, F. B. V., Baider, C., Seegobin, V. O. & Haugaasen, T. Invasive alien plant control improves foraging habitat quality of a threatened island flying fox. J. Nat. Conserv. 54, 125805 (2020).Article 

Google Scholar 
Monty, M. F., Florens, F. B. V. & Baider, C. Invasive alien plants elicit reduced production of flowers and fruits in various native forest species on the tropical island of Mauritius (Mascarenes, Indian Ocean). Trop. Conserv. Sci. 6, 35–49 (2013).Article 

Google Scholar 
Florens, F. B. V. & Baider, C. Ecological restoration in a developing island nation: how useful is the science? Restor. Ecol. 21, 1–5 (2013).Article 

Google Scholar 
Nogués-Bravo, D., Simberloff, D., Rahbek, C. & Sanders, N. J. Rewilding is the new Pandora’s box in conservation. Curr. Biol. 26, R87–R91 (2016).Article 
PubMed 

Google Scholar 
Linnebjerg, J. F., Hansen, D. M., Bunbury, N. & Olesen, J. M. Diet composition of the invasive red-whiskered bulbul Pycnonotus jocosus in Mauritius. J. Trop. Ecol. 26, 347–350 (2010).Article 

Google Scholar 
Sperry, J. H. et al. Fruit and seed traits of native and invasive plant species in Hawai’i: implications for seed dispersal by non-native birds. Biol. Invasions 23, 1819–1835 (2021).Article 

Google Scholar 
Hansen, D. M., Donlan, C. J., Griffiths, C. J. & Campbell, K. J. Ecological history and latent conservation potential: large and giant tortoises as a model for taxon substitutions. Ecography 33, 272–284 (2010).
Google Scholar 
Oleksy, R. Z. et al. The movement ecology of the Mauritian flying fox (Pteropus niger): a long-term study using solar-powered GSM/GPS tags. Mov. Ecol. 7, 1–12 (2019).Article 

Google Scholar 
Seegobin, V. O., Oleksy, R. Z. & Florens, F. B. V. Foraging and roosting patterns of a repeatedly mass-culled island flying fox offer avenues to mitigate human-wildlife conflict. Biodiversity 23, 49–60 (2022).Article 

Google Scholar 
Baider, C. et al. Status of plant conservation in oceanic islands of the Western Indian Ocean. In Proceedings of the 4th Global Botanic Gardens Congress (National Botanic Gardens of Ireland, Dublin, 2010).Humphreys, A. M., Govaerts, R., Ficinski, S. Z., Lughadha, E. N. & Vorontsova, M. S. Global dataset shows geography and life form predict modern plant extinction and rediscovery. Nat. Ecol. Evol. 3, 1043–1047 (2019).Article 
PubMed 

Google Scholar 
BGCI. State of the World’s Trees (BGCI, 2021).Vázquez-Yanes, C. & Orozco-Segovia, A. Patterns of seed longevity and germination in the tropical rainforest. Annu. Rev. Ecol. Syst. 24, 69–87 (1993).Article 

Google Scholar 
Gallaher, T., Callmander, M. W., Buerki, S. & Keeley, S. C. A long distance dispersal hypothesis for the Pandanaceae and the origins of the Pandanus tectorius complex. Mol. Phylogenet. Evol. 83, 20–32 (2015).Article 
PubMed 

Google Scholar 
Hansen, D. M., Kaiser, C. N. & Müller, C. B. Seed dispersal and establishment of endangered plants on oceanic islands: the Janzen-Connell model, and the use of ecological analogues. PLoS ONE 3, e2111 (2008).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
Albert, S., Flores, O., Stahl, M., Guilhabert, F. & Strasberg, D. Tree recruitment after native frugivore extinction? A field experiment to test the impact of fruit flesh persistence in a tropical oceanic island. J. Trop. Ecol. 38, 370–376 (2022).Article 

Google Scholar 
Witmer, M. C. & Cheke, A. S. The dodo and the tambalacoque tree: an obligate mutualism reconsidered. Oikos 61, 133–137 (1991).Bosser, J., Cadet, T., Guého, J. & Marais, W. Flore des Mascareignes: La Réunion, Maurice, Rodrigues (MSIRI/ORSTOM-IRD/Kew, Mauritius, 1976-onwards).Jordano, P. Fruits and frugivory. In Seeds: The Ecology of Regeneration in Plant Communities (ed. Fenner, N.) 125–165 (CABI Publishing, 2000).van der Pijl, L. Principles of Dispersal in Higher Plants 218 (Springer-Verlag, 1969).Dominy, N. J., Svenning, J. C. & Li, W. H. Historical contingency in the evolution of primate color vision. J. Hum. Evol. 44, 25–45 (2003).Article 
PubMed 

Google Scholar 
Oba, S. et al. A Bayesian missing value estimation method for gene expression profile data. Bioinformatics 19, 2088–2096 (2003).Article 
CAS 
PubMed 

Google Scholar 
Stekhoven, D. J. & Bühlmann, P. MissForest—non-parametric missing value imputation for mixed-type data. Bioinformatics 28, 112–118 (2012).Article 
CAS 
PubMed 

Google Scholar 
Qian, H. & Jin, Y. An updated megaphylogeny of plants, a tool for generating plant phylogenies and an analysis of phylogenetic community structure. J. Plant Ecol. 9, 233–239 (2016).Article 

Google Scholar 
Jin, Y. & Qian, H. V.PhyloMaker: an R package that can generate very large phylogenies for vascular plants. Ecography 42, 1353–1359 (2019).Article 

Google Scholar 
Santos, T., Diniz-Filho, J. A., e Luis, T. R., Bini, M., & Santos, M. T. Package ‘PVR’. Phylogenetic Eigenvectors Regression and Phylogentic Signal-Representation, 3274 (2018).Hume, J. P. Extinct Birds 2nd edn (Bloomsbury, 2017).Safford, R. & Hawkins, F. The Birds of Africa: Volume VIII: The Malagasy Region: Madagascar, Seychelles, Comoros, Mascarenes 960 (Bloomsbury Publishing, 2013).Albert, S., Flores, O., Ah-Peng, C. & Strasberg, D. Forests without frugivores and frugivores without forests—an investigation into the causes of a paradox in one of the last archipelagos colonized by humans. Front. Ecol. Evol. 9, 539 (2021).Albert, S. et al. Rediscovery of the mistletoe Bakerella hoyifolia subsp. bojeri (Loranthaceae) on Reunion Island: population status assessment for its conservation. Bot. Lett. 164, 229–236 (2017).Article 

Google Scholar 
Atkinson, R. & Sevathian, J.-C. A Guide to the Plants in Mauritius 188 (Mauritian Wildlife Foundation, 2005).Austin, J. J. & Arnold, E. N. Using ancient and recent DNA to explore relationships of extinct and endangered Leiolopisma skinks (Reptilia: Scincidae) in the Mascarene islands. Mol. Phylogenet. Evol. 39, 503–511 (2006).Article 
CAS 
PubMed 

Google Scholar 
Bissessur, P., Probst, J.-M. & Florens, F. B. V. Le Merle noir ou Bulbul de Maurice Hypsipetes olivaceus. Bull. Phaethon 46, 86–90 (2017).
Google Scholar 
Bullock, D. J. The ecology and conservation of reptiles on Round Island and Gunner’s Quion, Mauritius. Biol. Conserv. 37, 135–156 (1986).Article 

Google Scholar 
Cadet, L. J. T. La végétation de l’ile de La Réunion. Etude phytoécologique et phytosociologique. PhD thesis, Université Aix-Marseille, France, 362 (1977).Cheke, A. S. The ecology of the smaller land-birds of Mauritius. In Studies of Mascarene Islands Birds (ed. Diamond, A. W.) 151–207 (Cambridge University Press, 1987).Cole, R., Ladkoo, A., Tatayah, V. & Jones, C. Mauritius Olive White-eye Recovery Programme 2007-08 (Mauritian Wildlife Foundation, Vacoas, Mauritius, 2008).Falcón, W., Moll, D. & Hansen, D. M. Frugivory and seed dispersal by chelonians: a review and synthesis. Biol. Rev. 95, 142–166 (2020).Article 
PubMed 

Google Scholar 
Guérin, R. Faune ornithologique ancienne et actuelle des îles Mascareignes, Seychelles, Comores et des îles avoisinantes, Vol. 3 (General Printing & Stationery Co., 1940–53).Günther, A. C. L. G. The Gigantic Land-tortoises (Living and Extinct) in the Collection of the British Museum 96 (Order of the Trustees, London, 1877).Hansen, D. M. Ecology, Evolution, and Conservation of Plant-Animal Interactions in Islands. PhD thesis, University of Zurich, 192 (2006).Hansen, D. M. & Müller, C. B. Invasive ants disrupt gecko pollination and seed dispersal of the endangered plant Roussea simplex in Mauritius. Biotropica 41, 202–208 (2009).Article 

Google Scholar 
Harper, G. A. & Bunbury, N. Invasive rats on tropical islands: their population biology and impacts on native species. Glob. Ecol. Conserv. 3, 607–627 (2015).Article 

Google Scholar 
Henkel, F. W. & Schmidt, W. Amphibians and Reptiles of Madagascar and the Mascarene, Seychelles, and Comoro Islands 316 (Krieger Publishing, 2000).Hume, J. P. Systematics, morphology, and ecology of pigeons and doves (Aves: Columbidae) of the Mascarene Islands, with three new species. Zootaxa 3124, 1–62 (2011).Article 

Google Scholar 
Hume, J. P. Systematics, morphology, and ecology of rails (Aves: Rallidae) of the Mascarene Islands, with one new species. Zootaxa 4626, 001–107 (2019).Article 

Google Scholar 
Jones, C. G. The larger land-birds of Mauritius. In Studies of Mascarene Island birds (ed. Diamond, A. W.) 208–300 (Cambridge University Press, 1987).Jones, C. G. Studies on the Biology of the Pink Pigeon. Columba mayeri. PhD thesis, University College of Swansea, University of Wales, UK (1995).Larosa, A. M., Smith, C. W. & Gardner, D. E. Role of alien and native birds in the dissemination of firetree (Myrica faya Ait.-Myriacaceae) and associated plants in Hawaii. Pac. Sci. 39, 372–378 (1985).
Google Scholar 
Leguat de la Fougère, F. Voyage et aventures de François Leguat et de ses compagnons en deux iles désertes des Indes Orientales, Vol. 2 (J.J. Delorme, Amsterdam, 1707).Linnebjerg, J. F., Hansen, D. M. & Olesen, J. M. Gut passage effect of the introduced red-whiskered bulbul (Pycnonotus jocosus) on germination of invasive plant species in Mauritius. Austral. Ecol. 34, 272–277 (2009).Article 

Google Scholar 
Lorence, D. H. A monograph of the Monimiaceae (Laurales) in the Malagasy region (southwest Indian Ocean). Ann. Mo. Bot. Gard. 72, 1–165 (1985).Article 

Google Scholar 
Maggs, G. et al. Quantifying drivers of supplementary food use by a reintroduced, critically endangered passerine to inform management and habitat restoration. Biol. Conserv. 238, 108240 (2019).Article 

Google Scholar 
Meyer, J. Y. & Butaud, J. F. The impacts of rats on the endangered native flora of French Polynesia (Pacific Islands): drivers of plant extinction or coup de grâce species? Biol. Invasions 11, 1569–1585 (2009).Article 

Google Scholar 
Moorhouse-Gann, R. J. et al. New universal ITS2 primers for high-resolution herbivory analyses using DNA metabarcoding in both tropical and temperate zones. Sci. Rep. 8, 1–15 (2018).Article 
CAS 

Google Scholar 
Nyhagen, D. F., Kragelund, C., Olesen, J. M. & Jones, C. G. Insular interactions between lizards and flowers: flower visitation by an endemic Mauritian gecko. J. Trop. Ecol. 17, 755–761 (2001).Article 

Google Scholar 
Nyhagen, D. F., Turnbull, S. D., Olesen, J. M. & Jones, C. G. An investigation into the role of the Mauritian flying fox, Pteropus niger, in forest regeneration. Biol. Conserv. 122, 491–497 (2005).Article 

Google Scholar 
Probst, J.-M. Les Bulbuls du genre Hypsipetes dans les Mascareignes (Océan Indien). Observations Mascarines 1, 34–36 (1988).
Google Scholar 
Probst, J. M. Capacité de vol étonnante du Bulbul orphée Pycnonotus jocosus (Ile aux Aigrettes–Ile Maurice). Bull. Phaethon 1, 14–17 (1995).
Google Scholar 
Safford, R. Conservation of the Forest-living Native Birds of Mauritius. PhD thesis, University of Kent at Canterbury, 265 (1994).Sengupta, S. Food and feeding ecology of the common myna, Acridotheres tristis (Linn.). J. Proc. Indian Natl Sci. Acad. Part B Biol. Sci. 42, 338–345 (1976).
Google Scholar 
Staub, F. Evolutionary trends in some Mauritian phanerogams in relation to their pollinators. Proc. R. Soc. Arts Sci. Maurit. 5, 7–78 (1988).
Google Scholar 
Strahm, W. A. The Conservation and Restoration of the Flora of Mauritius and Rodrigues, Vol. 2. PhD thesis, University of Reading (1993) .Sussman, R. W. & Tattersall, I. Behavior and ecology of Macaca fascicularis in Mauritius: a preliminary study. Primates 22, 192–205 (1981).Article 

Google Scholar 
Sussman, R. W. & Tattersall, I. Distribution, abundance, and putative ecological strategy of Macaca fascicularis on the island of Mauritius, southwestern Indian Ocean. Folia Primatol. 46, 28–43 (1986).Article 

Google Scholar 
Valido, A. & Olesen, J. M. The importance of lizards as frugivores and seed dispersers. In Seed Dispersal: Theory and Its Application in a Changing World (eds Dennis, A. J. et al.) 124–147 (CAB International, 2007).Vinson, J. & Vinson, J. M. Notes on the reptiles of Round Island. Maurit. Inst. Bull. 8, 49–67 (1975).
Google Scholar 
von Bethlenfalvy, G. Vertebrate Seed Dispersers in Mauritius: Fruit Traits and Fruit Traits Preferences. MSc thesis, Institute of Zoology, University of Zurich, Switzerland (2006).Wilman, H. et al. EltonTraits 1.0: species-level foraging attributes of the world’s birds and mammals: ecological archives E095-178. Ecology 95, 2027–2027 (2014).Article 

Google Scholar 
Winters, R. & Hume, J. P. The dodo, the deer and a 1647 voyage to Japan. Historical. Biology 27, 258–264 (2015).
Google Scholar 
Zuël, N. Ecology and Conservation of an Endangered Reptile Community on Round Island, Mauritius. Doctoral dissertation, University of Zurich (2009).Zuël, N. et al. Ingestion by an endemic frugivore enhances seed germination of endemic plant species but decreases seedling survival of exotics. J. Biogeogr. 39, 2021–2030 (2012).Article 

Google Scholar 
Kissling, W. D., Böhning–Gaese, K. & Jetz, W. The global distribution of frugivory in birds. Glob. Ecol. Biogeogr. 18, 150–162 (2009).Article 

Google Scholar 
Sandom, C. et al. Mammal predator and prey species richness are strongly linked at macroscales. Ecology 94, 1112–1122 (2013).Article 
PubMed 

Google Scholar 
Hume, J. P. A new subfossil bulbul (Aves: Passerines: Pycnonotidae) from Rodrigues Island, Mascarenes, southwestern Indian Ocean. Ostrich 86, 247–260 (2015).Article 

Google Scholar 
Austin, J. J., Arnold, E. N. & Jones, C. G. Reconstructing an island radiation using ancient and recent DNA: the extinct and living day geckos (Phelsuma) of the Mascarene islands. Mol. Phylogenet. Evol. 31, 109–122 (2004).Article 
CAS 
PubMed 

Google Scholar 
Paradis, E. & Schliep, K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528 (2019).Article 
CAS 
PubMed 

Google Scholar  More

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

Google Scholar  More

Animal collection and holding for this project was conducted under Marine Research Permit RE-19–28 issued by the Ministry of Natural Resources, Environment, and Tourism of the Republic of Palau (10.03.2019), Marine Research/Collection Permit and Agreement 62 issued by the Koror State Government (08.10.2019), Queensland Government GBRMPA Marine Parks Permit G14/36689.1, Queensland Government DNPRSR Marine Parks Permits QS2014/MAN247 and QS2014/MAN247a, Queensland Government General Fisheries Permit 168991, Queensland Government DAFF Animal Ethics approval CA2013/11/733, approval by The Bahamas Department of Marine Resources, approval by the Animal Care Officer of both the University of Bremen and the Leibniz Centre for Tropical Marine Research (ZMT), and in accordance with UK and Germany animal care guidelines.Sample collectionWe collected fish carbonate samples at four study locations across three tropical and subtropical regions: Eleuthera (24°50’N, 76°20’W), The Bahamas, between 2009 and 201127,37; Heron Reef (23°27’S, 151°55’E) and Moreton Bay (27°29’S, 153°24’E) in Queensland, Australia, in 2014 and 201528; and Koror (7°20’N, 134°28’E), Palau, during November and December 2019. These are located within four distinct marine biogeographic provinces and three realms (Tropical Atlantic, Central Indo-Pacific, and Temperate Australasia)43. At each location fish were collected using barrier nets, dip nets, clove oil or hook and line, and immediately transferred to aquaria facilities at the Cape Eleuthera Institute, Heron Island and Moreton Bay Research Stations, and the Palau International Coral Reef Center. Fish were held in a range of tanks (60, 400, or 1400 L in the Bahamas, 10, 60, 100, 120, or 400 L in Heron Island and Moreton Bay, and 8, 80, 280, or 400 L in Palau) of suitable dimensions for different fish sizes ( 5). Each sample was titrated with 0.01–0.5 N HCl (with continuous aeration with CO2-free air) until the end point (grey-lavender; pH~4.80) was reached and stable for at least 10 min. If the sample was over-titrated (pink), 0.01–0.1 N NaOH was added to titrate back to the end point and the amount of base used was subtracted from the amount of acid. Acid and base were added using an electronic multi-dispenser pipette (Eppendorf Repeater ®E3X, Eppendorf, Hamburg, Germany) with a precision of  ± 1 ({{{{{rm{mu }}}}}})L. Additionally, the pH of several samples was monitored using a pH microelectrode (Mettler Toledo InLab Micro) to ascertain the correctness of the colorimetric end point. The amount of carbonate in the sample was then calculated using Eq. (1). The method was validated using certified reference material (Alkalinity Standard Solution, 25,000 mg/L as CaCO3, HACH) and the accuracy in the determination of solid samples was verified using certified CaCO3 powder (Suprapur, ≥ 99.95% purity, Merck) samples (60–500 ({{{{{rm{mu }}}}}})g) and resulted in 96.53 ± 1.94% accuracy (mean ± SE; n = 8).To compare values obtained with the two titration methods we further analysed 12 samples collected at Lizard Island, Australia, in February 2016. Samples were collected at 24 h intervals from one individual of Lethrinus atkinsoni (f. Lethrinidae, body mass: 245 g), a group of five Lutjanus fulvus (f. Lutjanidae, mean body mass: 21 g), and an individual of Cephalopholis cyanostigma (f. Serranidae, body mass: 295 g), following the procedures described above. During sample collection water temperature ranged from 29.1 °C during the night to 32.6 °C during the day, with an average of ~31 °C, mean salinity was 35.4, and pHNBS ranged from 8.13 to 8.21. To compare the amount of carbonate measured by the two methods we added carbonate samples to 20 ml ultrapure water and disaggregated crystals via sonication. We then used a Metrohm Titrando autotitrator and Metrohm Aquatrode pH electrode to measure initial pH of the suspension of carbonates, then titrated each sample of carbonate in two stages. Firstly, they were titrated down to pH 4.80 using 0.1 M HCl, adding 20 µl increments of acid until this was sufficient to keep pH below 4.80 for 10 min whilst bubbling with CO2-free air. This first stage was comparable to the single end point titration used for samples collected in Palau. Secondly, whilst continuing to bubble with CO2-free air, further acid was added to the sample until it reached pH 3.89 and was stable for 1 min. Then 0.1 M NaOH was added to the samples to return them to the initial pH. For all samples the first end point titration (to pH 4.80) yielded slightly higher values for carbonate content than the second double titration. The ratio between the two methods (single end point/double titration) was 1.08 ± 0.01 (mean ± SE; range: 1.04–1.14; Supplementary Table 2). As we found a small but consistent difference between the two methods, all following analyses were initially performed on the actual data obtained with the double titration for samples from Australia and The Bahamas, and the single end point titration for samples from Palau. Then, to assess the robustness of the results, we repeated the analyses after applying a correction factor of 1.08 to the excretion rates of Palauan fishes (that used the single end point titration method). All results were consistent and robust to the measured difference between the titration methods (Supplementary Figs. 8, 9).Finally, measurements of multiple samples from each individual collected over periods of 18–169 h (median: 64 h) were combined to produce an average individual excretion rate in ({{{{{rm{mu }}}}}})mol h−1. For fish held in groups, carbonate excretion rates per individual (of average biomass) were obtained by averaging the total excretion rate of the group across the sampling period and dividing it by the number of individuals in the tank. Excretion rates obtained from fish groups thus evened the intraspecific variability within tanks, and are therefore more robust than those directly obtained from fish held individually. This aspect was considered in our models by fitting weighted regressions (see the “Statistical modelling” section). In total, we measured the carbonate excretion rates of 382 individual fishes arranged in 192 groups (i.e., independent observations), representing 85 species from 35 families across three tropical regions (180 individuals from 29 species in Australia, 90 individuals from 10 species in the Bahamas, and 112 individuals from 46 species in Palau; Supplementary Table 1).We assume that during the sampling of carbonates fishes were close to their resting metabolic rate and that their carbonate excretion rates are representative of fish at rest. Although the ratio of tank volume to fish volume in our study (median ~660; inter-quartile range ~180–1700) typically greatly exceeds the guideline ideal range for measuring resting metabolic rate (20–50)85, fishes were fasted prior to and throughout sampling, and in most instances their movement was somewhat constrained by tank volume. Fasting reduces metabolic rate in all animals, including fish, as they do not undergo energy-intensive digestive processes and use energy reserves to support vital processes, triggering metabolic changes in many tissues and reducing activity levels86,87. Additionally, other than the carbonate syphoning ( More

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

Strains belonging to the same species display distinct growth dynamics on the marine polysaccharide alginateWe first quantified the growth dynamics of the 12 Vibrionaceae strains (Supplementary Table 1) on alginate in well-mixed batch cultures. Growth of populations was initiated at approximately the same inoculum density (105 colony forming units (c.f.u.) ml−1). We tracked the growth dynamics by measuring the optical density at 600 nm and compared the maximum population size reached over the course of 36 h (Fig. 1 and S1). We found significant differences in the maximal optical density achieved by different strains within each species (Fig. 1 and S1). In V. splendidus, strains 12B01 and FF6 reached a lower maximum population size compared to strains 1S124 and 13B01 (Fig. 1 and S1A). In V. cyclitrophicus, strain ZF270 reached a lower maximum population size compared to strains 1F175, 1F111, and ZF28 (Fig. 1 and S1A). Similarly, in V. sp. F13, strain 9ZC77 reached a lower maximum population size than strains 9CS106, 9ZC13, and ZF57 (Fig. 1 and S1A). These findings suggest that some strains are limited in their growth abilities in well-mixed environments, perhaps as a consequence of differences in the amount and activity of enzymes they release (Supplementary Table 1).Fig. 1: Vibrionaceae strains differ in their growth dynamics on the marine polysaccharide alginate under well-mixed conditions.Maximum optical density (measured at 600 nm) achieved by populations of strains belonging to Vibrio splendidus, Vibrio cyclitrophicus, and Vibrio sp. F13 during the course of a 36 h growth cycle on the same concentration (0.1% weight/volume) of the polysaccharide alginate. Points and error bars indicate the mean of measurements across populations within each ecotype (npopulations = 3) and the 95% confidence interval (CI), respectively. Different letters indicate statistically significant differences between strains within one species (One-way ANOVA and Dunnett’s post-hoc test; V. splendidus: p  More

Benca, J. P., Duijnstee, I. A. & Looy, C. V. Fossilized pollen malformations as indicators of past environmental stress and meiotic disruption: Insights from modern conifers. Paleobiology, 1–34 (2022).Marshall, J. E., Lakin, J., Troth, I. & Wallace-Johnson, S. M. Uv-b radiation was the devonian-carboniferous boundary terrestrial extinction kill mechanism. Sci. Adv. 6, eaba0768 (2020).Article 
ADS 
CAS 

Google Scholar 
Looy, C. V., Twitchett, R. J., Dilcher, D. L., Van Konijnenburg-Van Cittert, J. H. & Visscher, H. Life in the end-permian dead zone. Proc. Natl. Acad. Sci. 98, 7879–7883 (2001).Article 
ADS 
CAS 

Google Scholar 
Foster, C. & Afonin, S. Abnormal pollen grains: An outcome of deteriorating atmospheric conditions around the permian-triassic boundary. J. Geol. Soc. 162, 653–659 (2005).Article 
ADS 

Google Scholar 
Hochuli, P. A., Schneebeli-Hermann, E., Mangerud, G. & Bucher, H. Evidence for atmospheric pollution across the permian-triassic transition. Geology 45, 1123–1126 (2017).Article 
ADS 

Google Scholar 
Galasso, F., Bucher, H. & Schneebeli-Hermann, E. Mapping monstrosity: Malformed sporomorphs across the smithian/spathian boundary interval and beyond (salt range, pakistan). Global Planet. Change 219, 103975 (2022).Article 

Google Scholar 
Van de Schootbrugge, B. et al. Floral changes across the triassic/jurassic boundary linked to flood basalt volcanism. Nat. Geosci. 2, 589–594 (2009).Article 
ADS 

Google Scholar 
Lindström, S. et al. Volcanic mercury and mutagenesis in land plants during the end-triassic mass extinction. Sci. Adv. 5, eaaw4018 (2019).Article 
ADS 

Google Scholar 
Gravendyck, J., Schobben, M., Bachelier, J. B. & Kürschner, W. M. Macroecological patterns of the terrestrial vegetation history during the end-triassic biotic crisis in the central european basin: A palynological study of the bonenburg section (nw-germany) and its supra-regional implications. Global Planet. Change 194, 103286 (2020).Article 

Google Scholar 
Vilas-Boas, M., Pereira, Z., Cirilli, S., Duarte, L. V. & Fernandes, P. New data on the palynology of the triassic-jurassic boundary of the silves group, lusitanian basin, portugal. Rev. Palaeobot. Palynol. 290, 104426 (2021).Article 

Google Scholar 
Galasso, F., Feist-Burkhardt, S. & Schneebeli-Hermann, E. The palynology of the toarcian oceanic anoxic event at dormettingen, southwest germany, with emphasis on changes in vegetational dynamics. Rev. Palaeobotany Palynol. 304, 104701 (2022).Article 

Google Scholar 
Galasso, F., Feist-Burkhardt, S. & Schneebeli-Hermann, E. Do spores herald the toarcian oceanic anoxic event?. Rev. Palaeobot. Palynol. 306, 104748 (2022).Article 

Google Scholar 
Hay, W. W. & Floegel, S. New thoughts about the cretaceous climate and oceans. Earth Sci. Rev. 115, 262–272 (2012).Article 
ADS 
CAS 

Google Scholar 
Faucher, G., Erba, E., Bottini, C. & Gambacorta, G. Calcareous nannoplankton response to the latest cenomanian oceanic anoxic event 2 perturbation. RIVISTA ITALIANA DI PALEONTOLOGIA E STRATIGRAFIA (2017).Cohen, K. M., Finney, S. C., Gibbard, P. L. & Fan, J.-X. The ics international chronostratigraphic chart. Epis. J. Int. Geosci. 36, 199–204 (2013).
Google Scholar 
Caron, M. & Homewood, P. Evolution of early planktic foraminifers. Mar. Micropaleontol. 7, 453–462 (1983).Article 
ADS 

Google Scholar 
Jarvis, I. et al. Microfossil assemblages and the cenomanian-turonian (late cretaceous) oceanic anoxic event. Cretac. Res. 9, 3–103 (1988).Article 

Google Scholar 
Huber, B. T., Leckie, R. M., Norris, R. D., Bralower, T. J. & CoBabe, E. Foraminiferal assemblage and stable isotopic change across the cenomanian-turonian boundary in the subtropical north atlantic. J. Foraminiferal Res. 29, 392–417 (1999).
Google Scholar 
Culver, S. J. & Rawson, P. F. Biotic response to global change: The last 145 million years (Cambridge University Press, 2006).Erba, E. Calcareous nannofossils and mesozoic oceanic anoxic events. Mar. Micropaleontol. 52, 85–106 (2004).Article 
ADS 

Google Scholar 
Gebhardt, H., Kuhnt, W. & Holbourn, A. Foraminiferal response to sea level change, organic flux and oxygen deficiency in the cenomanian of the tarfaya basin, southern morocco. Mar. Micropaleontol. 53, 133–157 (2004).Article 
ADS 

Google Scholar 
Hardenbol, J. et al. Mesozoic and cenozoic sequence chronostratigraphic framework of european basins. Soc. Sediment. Geol. (1998).Miller, K. G. et al. The phanerozoic record of global sea-level change. Science 310, 1293–1298 (2005).Article 
ADS 
CAS 

Google Scholar 
Voigt, S., Gale, A. S. & Voigt, T. Sea-level change, carbon cycling and palaeoclimate during the late cenomanian of northwest europe; an integrated palaeoenvironmental analysis. Cretac. Res. 27, 836–858 (2006).Article 

Google Scholar 
Haq, B. U. Cretaceous eustasy revisited. Global Planet. Change 113, 44–58 (2014).Article 
ADS 

Google Scholar 
Sames, B. et al. Short-term sea-level changes in a greenhouse world-a view from the cretaceous. Palaeogeogr. Palaeoclimatol. Palaeoecol. 441, 393–411 (2016).Article 

Google Scholar 
Arthur, M. A., Dean, W. E. & Pratt, L. M. Geochemical and climatic effects of increased marine organic carbon burial at the cenomanian/turonian boundary. Nature 335, 714–717 (1988).Article 
ADS 

Google Scholar 
Tsikos, H. et al. Carbon-isotope stratigraphy recorded by the cenomanian-turonian oceanic anoxic event: Correlation and implications based on three key localities. J. Geol. Soc. 161, 711–719 (2004).Article 
ADS 
CAS 

Google Scholar 
Jarvis, I., Lignum, J. S., Gröcke, D. R., Jenkyns, H. C. & Pearce, M. A. Black shale deposition, atmospheric co2 drawdown, and cooling during the cenomanian-turonian oceanic anoxic event. Paleoceanography26 (2011).van Bentum, E. C., Reichart, G.-J. & Damsté, J. S. S. Organic matter provenance, palaeoproductivity and bottom water anoxia during the cenomanian/turonian oceanic anoxic event in the newfoundland basin (northern proto north atlantic ocean). Org. Geochem. 50, 11–18 (2012).Article 

Google Scholar 
Owens, J. D., Lyons, T. W. & Lowery, C. M. Quantifying the missing sink for global organic carbon burial during a cretaceous oceanic anoxic event. Earth Planet. Sci. Lett. 499, 83–94 (2018).Article 
ADS 
CAS 

Google Scholar 
Bralower, T. J. Calcareous nannofossil biostratigraphy and assemblages of the cenomanian-turonian boundary interval: Implications for the origin and timing of oceanic anoxia. Paleoceanography 3, 275–316 (1988).Article 
ADS 

Google Scholar 
Leckie, R. M., Bralower, T. J. & Cashman, R. Oceanic anoxic events and plankton evolution: Biotic response to tectonic forcing during the mid-cretaceous. Paleoceanography 17, 13–1 (2002).Article 

Google Scholar 
Slater, S. M., Bown, P., Twitchett, R. J., Danise, S. & Vajda, V. Global record of “ghost’’ nannofossils reveals plankton resilience to high co2 and warming. Science 376, 853–856 (2022).Article 
ADS 
CAS 

Google Scholar 
Forster, A., Schouten, S., Moriya, K., Wilson, P. A. & Sinninghe Damsté, J. S. Tropical warming and intermittent cooling during the cenomanian/turonian oceanic anoxic event 2: Sea surface temperature records from the equatorial atlantic. Paleoceanography22 (2007).Barclay, R. S., McElwain, J. C. & Sageman, B. B. Carbon sequestration activated by a volcanic co2 pulse during ocean anoxic event 2. Nat. Geosci. 3, 205–208 (2010).Article 
ADS 
CAS 

Google Scholar 
Damsté, J. S. S., van Bentum, E. C., Reichart, G.-J., Pross, J. & Schouten, S. A co2 decrease-driven cooling and increased latitudinal temperature gradient during the mid-cretaceous oceanic anoxic event 2. Earth Planet. Sci. Lett. 293, 97–103 (2010).Article 
ADS 

Google Scholar 
Heimhofer, U. et al. Vegetation response to exceptional global warmth during oceanic anoxic event 2. Nat. Commun. 9, 1–8 (2018).Article 
CAS 

Google Scholar 
Huber, B. T., MacLeod, K. G., Watkins, D. K. & Coffin, M. F. The rise and fall of the cretaceous hot greenhouse climate. Global Planet. Change 167, 1–23 (2018).Article 
ADS 

Google Scholar 
Robinson, S. A. et al. Southern hemisphere sea-surface temperatures during the cenomanian-turonian: Implications for the termination of oceanic anoxic event 2. Geology 47, 131–134 (2019).Article 
ADS 
CAS 

Google Scholar 
Voigt, S., Gale, A. S. & Flögel, S. Midlatitude shelf seas in the cenomanian-turonian greenhouse world: Temperature evolution and north atlantic circulation. Paleoceanography19 (2004).Van Helmond, N. et al. Freshwater discharge controlled deposition of cenomanian-turonian black shales on the nw european epicontinental shelf (wunstorf, north germany). Clim. Past Discuss 10, 3755–3786 (2014).ADS 

Google Scholar 
Li, Y.-X., Montanez, I. P., Liu, Z. & Ma, L. Astronomical constraints on global carbon-cycle perturbation during oceanic anoxic event 2 (oae2). Earth Planet. Sci. Lett. 462, 35–46 (2017).Article 
ADS 
CAS 

Google Scholar 
O’Brien, C. L. et al. Cretaceous sea-surface temperature evolution: Constraints from tex86 and planktonic foraminiferal oxygen isotopes. Earth Sci. Rev. 172, 224–247 (2017).Article 
ADS 

Google Scholar 
Jones, C. E. & Jenkyns, H. C. Seawater strontium isotopes, oceanic anoxic events, and seafloor hydrothermal activity in the jurassic and cretaceous. Am. J. Sci. 301, 112–149 (2001).Article 
ADS 
CAS 

Google Scholar 
Snow, L. J., Duncan, R. A. & Bralower, T. J. Trace element abundances in the rock canyon anticline, pueblo, colorado, marine sedimentary section and their relationship to caribbean plateau construction and oxygen anoxic event 2. Paleoceanography20 (2005).Kuroda, J. et al. Contemporaneous massive subaerial volcanism and late cretaceous oceanic anoxic event 2. Earth Planet. Sci. Lett. 256, 211–223 (2007).Article 
ADS 
CAS 

Google Scholar 
Turgeon, S. C. & Creaser, R. A. Cretaceous oceanic anoxic event 2 triggered by a massive magmatic episode. Nature 454, 323–326 (2008).Article 
ADS 
CAS 

Google Scholar 
Floegel, S. et al. Simulating the biogeochemical effects of volcanic co2 degassing on the oxygen-state of the deep ocean during the cenomanian/turonian anoxic event (oae2). Earth Planet. Sci. Lett. 305, 371–384 (2011).Article 
ADS 
CAS 

Google Scholar 
Tegner, C. et al. Magmatism and eurekan deformation in the high arctic large igneous province: 40ar-39ar age of kap washington group volcanics, north greenland. Earth Planet. Sci. Lett. 303, 203–214 (2011).Article 
ADS 
CAS 

Google Scholar 
Du Vivier, A. D. et al. Marine 187os/188os isotope stratigraphy reveals the interaction of volcanism and ocean circulation during oceanic anoxic event 2. Earth Planet. Sci. Lett. 389, 23–33 (2014).Article 
ADS 

Google Scholar 
Du Vivier, A., Selby, D., Condon, D., Takashima, R. & Nishi, H. Pacific 187os/188os isotope chemistry and u-pb geochronology: Synchroneity of global os isotope change across oae 2. Earth Planet. Sci. Lett. 428, 204–216 (2015).Article 
ADS 

Google Scholar 
Meyers, P. A. Why are the (delta )13corg values in phanerozoic black shales more negative than in modern marine organic matter?. Geochem. Geophys. Geosyst. 15, 3085–3106 (2014).Article 
ADS 
CAS 

Google Scholar 
Jenkyns, H. C., Dickson, A. J., Ruhl, M. & Van den Boorn, S. H. Basalt-seawater interaction, the plenus cold event, enhanced weathering and geochemical change: Deconstructing oceanic anoxic event 2 (cenomanian-turonian, late cretaceous). Sedimentology 64, 16–43 (2017).Article 
CAS 

Google Scholar 
Scaife, J. et al. Sedimentary mercury enrichments as a marker for submarine large igneous province volcanism? evidence from the mid-cenomanian event and oceanic anoxic event 2 (late cretaceous). Geochem. Geophys. Geosyst. 18, 4253–4275 (2017).Article 
ADS 
CAS 

Google Scholar 
Schröder-Adams, C. J., Herrle, J. O., Selby, D., Quesnel, A. & Froude, G. Influence of the high arctic igneous province on the cenomanian/turonian boundary interval, sverdrup basin, high canadian arctic. Earth Planet. Sci. Lett. 511, 76–88 (2019).Article 
ADS 

Google Scholar 
Jolet, P., Philip, J., Thomel, G., Lopez, G. & Tronchetti, G. Nouvelles données biostratigraphiques sur la limite cénomanien-turonien. la coupe de cassis (sud-est de la france): Proposition d’un hypostratotype européen. Comptes Rendus de l’Académie des Sciences-Series IIA-Earth and Planetary Science325, 703–709 (1997).Bown, P. R. & Young, J. Calcareous nannofossil biostratigraphy (Springer, 1998).Green, T., Renne, P. R. & Keller, C. B. Continental flood basalts drive phanerozoic extinctions. Proc. Natl. Acad. Sci. 119, e2120441119 (2022).Article 
CAS 

Google Scholar 
Percival, L. M. et al. Does large igneous province volcanism always perturb the mercury cycle? Comparing the records of oceanic anoxic event 2 and the end-cretaceous to other mesozoic events. Am. J. Sci. 318, 799–860 (2018).Article 
ADS 
CAS 

Google Scholar 
Salazar, L. et al. Diversity patterns of ferns along elevational gradients in andean tropical forests. Plant Ecol. Divers. 8, 13–24 (2015).Article 

Google Scholar 
Mehltreter, K., Walker, L. R. & Sharpe, J. M. Fern ecology (Cambridge University Press, 2010).Carvajal-Hernández, C. I., Gómez-Díaz, J. A., Kessler, M. & Krömer, T. Influence of elevation and habitat disturbance on the functional diversity of ferns and lycophytes. Plant Ecol. Divers. 11, 335–347 (2018).Article 

Google Scholar 
Kürschner, W. M., Batenburg, S. J. & Mander, L. Aberrant classopollis pollen reveals evidence for unreduced (2 n) pollen in the conifer family cheirolepidiaceae during the triassic-jurassic transition. Proc. Royal Soc. B: Biol. Sci. 280, 20131708 (2013).Article 

Google Scholar 
Traverse, A. Paleopalynology Vol. 28 (Springer Science & Business Media, 2007).Tyson, R. V. Palynofacies investigation of callovian (middle jurassic) sediments from dsdp site 534, blake-bahama basin, western central atlantic. Mar. Pet. Geol. 1, 3–13 (1984).Article 

Google Scholar 
RV, T. Sedimentary organic matter: Organic facies and palynofacieschapman & hall. London, 615pp (1995).Vakhrameyev, V. Classopollis pollen as an indicator of jurassic and cretaceous climate. Int. Geol. Rev. 24, 1190–1196 (1982).Article 

Google Scholar 
Vakhrameev, V. Range and palaeoecology of mesozoic conifers, the cheirolepidiaceae. Paleontol. Zh. 1, 19–34 (1970).
Google Scholar 
WATSON, J. Some lower cretaceous conifers of the cheirolepidiaceae from the usa and england. Palaeontology 20, 715–749 (1977).
Google Scholar 
Fonseca, C., Mendonça Filho, J. G., Lézin, C., De Oliveira, A. D. & Duarte, L. V. Organic matter deposition and paleoenvironmental implications across the cenomanian-turonian boundary of the subalpine basin (se france): Local and global controls. Int. J. Coal Geol. 218, 103364 (2020).Article 
CAS 

Google Scholar 
Benca, J. P., Duijnstee, I. A. & Looy, C. V. Uv-b-induced forest sterility: Implications of ozone shield failure in earth’s largest extinction. Sci. Adv. 4, e1700618 (2018).Article 
ADS 

Google Scholar 
Wilson, L. A study in variation of picea glauca (moench) voss pollen. Grana 4, 380–387 (1963).
Google Scholar 
Lindström, S., McLoughlin, S. & Drinnan, A. N. Intraspecific variation of taeniate bisaccate pollen within permian glossopterid sporangia, from the prince charles mountains, antarctica. Int. J. Plant Sci. 158, 673–684 (1997).Article 

Google Scholar 
Leitch, A. & Leitch, I. Ecological and genetic factors linked to contrasting genome dynamics in seed plants. New Phytol. 194, 629–646 (2012).Article 
CAS 

Google Scholar 
Coffin, M. F. & Eldholm, O. Large igneous provinces: crustal structure, dimensions, and external consequences. Rev. Geophys. 32, 1–36 (1994).Article 
ADS 

Google Scholar 
Wignall, P. B. Large igneous provinces and mass extinctions. Earth Sci. Rev. 53, 1–33 (2001).Article 
ADS 
CAS 

Google Scholar 
McElwain, J. C., Wade-Murphy, J. & Hesselbo, S. P. Changes in carbon dioxide during an oceanic anoxic event linked to intrusion into gondwana coals. Nature 435, 479–482 (2005).Article 
ADS 
CAS 

Google Scholar 
Bond, D. P., Wignall, P. B., Keller, G. & Kerr, A. Large igneous provinces and mass extinctions: An update. Volcan., Impacts, Mass Extinc.: Causes Effects 505, 29–55 (2014).
Google Scholar 
Burgess, S., Bowring, S., Fleming, T. & Elliot, D. High-precision geochronology links the ferrar large igneous province with early-jurassic ocean anoxia and biotic crisis. Earth Planet. Sci. Lett. 415, 90–99 (2015).Article 
ADS 
CAS 

Google Scholar 
Burgess, S. D., Muirhead, J. D. & Bowring, S. A. Initial pulse of siberian traps sills as the trigger of the end-permian mass extinction. Nat. Commun. 8, 1–6 (2017).Article 
ADS 
CAS 

Google Scholar 
Ernst, R. E. & Youbi, N. How large igneous provinces affect global climate, sometimes cause mass extinctions, and represent natural markers in the geological record. Palaeogeogr. Palaeoclimatol. Palaeoecol. 478, 30–52 (2017).Article 

Google Scholar 
Ruhl, M. et al. Reduced plate motion controlled timing of early jurassic karoo-ferrar large igneous province volcanism. Sci. Adv. 8, eabo0866 (2022).Article 
CAS 

Google Scholar 
Dickens, G. R., Paull, C. K. & Wallace, P. Direct measurement of in situ methane quantities in a large gas-hydrate reservoir. Nature 385, 426–428 (1997).Article 
ADS 
CAS 

Google Scholar 
Courtillot, V. E. & Renne, P. R. On the ages of flood basalt events. C.R. Geosci. 335, 113–140 (2003).Article 
ADS 

Google Scholar 
Rampino, M. R., Rodriguez, S., Baransky, E. & Cai, Y. Global nickel anomaly links siberian traps eruptions and the latest permian mass extinction. Sci. Rep. 7, 1–6 (2017).Article 
CAS 

Google Scholar 
Clapham, M. E. & Renne, P. R. Flood basalts and mass extinctions. Annu. Rev. Earth Planet. Sci. 47, 275–303 (2019).Article 
ADS 
CAS 

Google Scholar 
McElwain, J. C., Popa, M. E., Hesselbo, S. P., Haworth, M. & Surlyk, F. Macroecological responses of terrestrial vegetation to climatic and atmospheric change across the triassic/jurassic boundary in east greenland. Paleobiology 33, 547–573 (2007).Article 

Google Scholar 
Van de Schootbrugge, B. et al. End-triassic calcification crisis and blooms of organic-walled ‘disaster species’. Palaeogeogr. Palaeoclimatol. Palaeoecol. 244, 126–141 (2007).Article 

Google Scholar 
Ruckwied, K., Götz, A. E., Pálfy, J. & Török, Á. Palynology of a terrestrial coal-bearing series across the triassic/jurassic boundary (mecsek mts, hungary). Central Euro. Geol. 51, 1–15 (2008).Article 
CAS 

Google Scholar 
Götz, A., Ruckwied, K., Pálfy, J. & Haas, J. Palynological evidence of synchronous changes within the terrestrial and marine realm at the triassic/jurassic boundary (csővár section, hungary). Rev. Palaeobot. Palynol. 156, 401–409 (2009).Article 

Google Scholar 
Hochuli, P. A., Hermann, E., Vigran, J. O., Bucher, H. & Weissert, H. Rapid demise and recovery of plant ecosystems across the end-permian extinction event. Global Planet. Change 74, 144–155 (2010).Article 
ADS 

Google Scholar 
Bonis, N. et al.Palaeoenvironmental changes and vegetation history during the Triassic-Jurassic transition (LPP Contribution Series No. 29, 2010).Bonis, N. R. & Kürschner, W. M. Vegetation history, diversity patterns, and climate change across the triassic/jurassic boundary. Paleobiology 38, 240–264 (2012).Article 

Google Scholar 
Visscher, H. et al. Environmental mutagenesis during the end-permian ecological crisis. Proc. Natl. Acad. Sci. 101, 12952–12956 (2004).Article 
ADS 
CAS 

Google Scholar  More