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    Adult sex ratios: causes of variation and implications for animal and human societies

    Wedekind, C. & Küng, C. Shift of spawning season and effects of climate warming on developmental stages of a grayling (Salmonidae). Conserv. Biol. 24, 1418–1423 (2010).PubMed 

    Google Scholar 
    Capdevila, P., Stott, I., Beger, M. & Salguero-Gómez, R. Towards a comparative framework of demographic resilience. Trends Ecol. Evol. 35, 776–786 (2020).PubMed 

    Google Scholar 
    Katzner, T. E. et al. Assessing population-level consequences of anthropogenic stressors for terrestrial wildlife. Ecosphere 11, e03046 (2020).
    Google Scholar 
    Zhou, X. & Hesketh, T. High sex ratios in rural China: declining well-being with age in never-married men. Philos. Trans. R. Soc. B: Biol. Sci. 372, 20160324 (2017). One of the few studies in humans that targets well-being as an outcome, showing concerning mental health implications of sex ratio skew.
    Google Scholar 
    Schacht, R., Rauch, K. L. & Borgerhoff Mulder, M. Too many men: the violence problem? Trends Ecol. Evol. 29, 214–222 (2014). An influential review of violence and sex ratios across human societies that sets the agenda how reformulated sexual selection theory can inform mating strategies in humans.PubMed 

    Google Scholar 
    Donald, P. F. Adult sex ratios in wild bird populations. Ibis 149, 671–692 (2007).
    Google Scholar 
    Székely, T., Weissing, F. J. & Komdeur, J. Adult sex ratio variation: implications for breeding system evolution. J. Evol. Biol. 27, 1500–1512 (2014). A comprehensive overview of mate choice, mating systems and parental care in relation to ASR.PubMed 

    Google Scholar 
    Du Bois, W. E. B. The Philadelphia Negro (The University of Pennsylvania, 1899).Groves, E. & Ogburn, W. American Marriage and Family Relationships (Henry Holt and Company, 1928).Mayr, E. The sex ratio in wild birds. Am. Naturalist 73, 156–179 (1939).
    Google Scholar 
    Trivers, R. L. Parental investment and sexual selection. in Sexual Selection & the Descent of Man 136–179 (Aldine de Gruyter, 1972).Kramer, K., Schacht, R. & Bell, A. Adult sex ratios and partner scarcity among hunter–gatherers: Implications for dispersal patterns and the evolution of human sociality. Philos. Trans. R. Soc. B: Biol. Sci. 372, 20160316 (2017).
    Google Scholar 
    Kappeler, P. M. et al. Sex roles and sex ratios in animals. Biol. Rev. (in press).Kappeler, P. M. Sex roles and adult sex ratios: insights from mammalian biology and consequences for primate behaviour. Philos. Trans. R. Soc. B: Biol. Sci. 372, 20160321 (2017).
    Google Scholar 
    Clutton-Brock, T. Social evolution in mammals. Science 373, eabc9699 (2021).PubMed 

    Google Scholar 
    Garamszegi, L. Z., Pavlova, D. Z., Eens, M. & Møller, A. P. The evolution of song in female birds in Europe. Behav. Ecol. 18, 86–96 (2007).
    Google Scholar 
    Cooney, C. R. et al. Sexual selection predicts the rate and direction of colour divergence in a large avian radiation. Nat. Commun. 10, 1773 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    Ancona, S., Dénes, F. V., Krüger, O., Székely, T. & Beissinger, S. R. Estimating adult sex ratios in nature. Philos. Trans. R. Soc. B: Biol. Sci. 372, 20160313 (2017). A methodology-focused review highlighting the pros and cons of various ASR estimation methods used in wildlife biology.
    Google Scholar 
    Fitze, P. S. & Le Galliard, J.-F. Operational sex ratio, sexual conflict and the intensity of sexual selection. Ecol. Lett. 11, 432–439 (2008).PubMed 

    Google Scholar 
    Kokko, H. & Jennions, M. D. Parental investment, sexual selection and sex ratios. J. Evolut. Biol. 21, 919–948 (2008). A landmark theoretical study that explains the complex relationships between parental care, ASR and OSR.
    Google Scholar 
    Emlen, S. T. & Oring, L. W. Ecology, sexual selection, and the evolution of mating systems. Science 197, 215–223 (1977). A landmark study that introduced the concept of operational sex ratio (OSR).PubMed 

    Google Scholar 
    Pipoly, I. et al. The genetic sex-determination system predicts adult sex ratios in tetrapods. Nature 527, 91–94 (2015). A pathbreaking phylogenetic study that showed sex determination systems are related to ASR in tetrapods.PubMed 

    Google Scholar 
    Carmona-Isunza, M. C. et al. Adult sex ratio and operational sex ratio exhibit different temporal dynamics in the wild. Behav. Ecol. 28, 523–532 (2017).
    Google Scholar 
    Weir, L., Grant, J. & Hutchings, J. The influence of operational sex ratio on the intensity of competition for mates. Am. Naturalist 177, 167–176 (2011).
    Google Scholar 
    Hays, G. C., Shimada, T. & Schofield, G. A review of how the biology of male sea turtles may help mitigate female-biased hatchling sex ratio skews in a warming climate. Mar. Biol. 169, 89 (2022).
    Google Scholar 
    Ancona, S., Liker, A., Carmona-Isunza, M. C. & Székely, T. Sex differences in age-to-maturation relate to sexual selection and adult sex ratios in birds. Evolution Lett. 4, 44–53 (2020).
    Google Scholar 
    Gluckman, P. D. & Hanson, M. A. Evolution, development and timing of puberty. Trends Endocrinol. Metab. 17, 7–12 (2006).PubMed 

    Google Scholar 
    Veran, S. & Beissinger, S. R. Demographic origins of skewed operational and adult sex ratios: perturbation analyses of two-sex models. Ecol. Lett. 12, 129–143 (2009).PubMed 

    Google Scholar 
    Wilson, E. O. Sociobiology: The New Synthesis. (Harvard University Press, 1975).Ågren, J. A. & Clark, A. G. Selfish genetic elements. PLoS Genet. 14, e1007700 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    Engelstädter, J. & Hurst, G. D. D. The ecology and evolution of microbes that manipulate host reproduction. Annu. Rev. Ecol., Evolution, Syst. 40, 127–149 (2009).
    Google Scholar 
    Beukeboom, L. W. & Perrin, N. The Evolution of Sex Determination. (Oxford University Press, 2014). https://doi.org/10.1093/acprof:oso/9780199657148.001.0001.Geffroy, B. & Douhard, M. The adaptive sex in stressful environments. Trends Ecol. Evol. 34, 628–640 (2019).PubMed 

    Google Scholar 
    Nemesházi, E. et al. Novel genetic sex markers reveal high frequency of sex reversal in wild populations of the agile frog (Rana dalmatina) associated with anthropogenic land use. Mol. Ecol. 29, 3607–3621 (2020).PubMed 

    Google Scholar 
    Geffroy, B. Energy as the cornerstone of environmentally driven sex allocation. Trends Endocrinol. Metab. 33, 670–679 (2022).PubMed 

    Google Scholar 
    Janzen, F. J. & Paukstis, G. L. Environmental sex determination in reptiles: ecology, evolution, and experimental design. Q Rev. Biol. 66, 149–179 (1991).PubMed 

    Google Scholar 
    Cook, J. M. Sex determination in invertebrates. in Sex Ratios: Concepts and Research Methods (ed. Hardy, I. C. W.) 178–194 (Cambridge University Press, 2002). https://doi.org/10.1017/CBO9780511542053.009.Godwin, J., Luckenbach, J. A. & Borski, R. J. Ecology meets endocrinology: environmental sex determination in fishes. Evol. Dev. 5, 40–49 (2003).PubMed 

    Google Scholar 
    West, S. Sex Allocation. (Princeton University Press, 2009).Geffroy, B. & Wedekind, C. Effects of global warming on sex ratios in fishes. J. Fish. Biol. 97, 596–606 (2020).PubMed 

    Google Scholar 
    Edmands, S. Sex ratios in a warming world: thermal effects on sex-biased survival, sex determination, and sex reversal. J. Heredity 112, 155–164 (2021).
    Google Scholar 
    Valenzuela, N. et al. Extreme thermal fluctuations from climate change unexpectedly accelerate demographic collapse of vertebrates with temperature-dependent sex determination. Sci. Rep. 9, 4254 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    Hays, G. C., Mazaris, A. D. & Schofield, G. Different male vs. female breeding periodicity helps mitigate offspring sex ratio skews in sea turtles. Front. Marine Sci. 1, 43 (2014).Maitre, D. et al. Sex differentiation in grayling (Salmonidae) goes through an all-male stage and is delayed in genetic males who instead grow faster. Sci. Rep. 7, 15024 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Donald, P. F. Lonely males and low lifetime productivity in small populations. Ibis 153, 465–467 (2011).
    Google Scholar 
    Mabry, K. E., Shelley, E. L., Davis, K. E., Blumstein, D. T. & Vuren, D. H. V. Social mating system and sex-biased dispersal in mammals and birds: a phylogenetic analysis. PLoS ONE 8, e57980 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    Clutton-Brock, T. Mammal Societies. (John Wiley and Sons, 2016).Kalmbach, E. & Benito, M. M. Sexual size dimorphism and offspring vulnerability in birds. in Sex, Size and Gender Roles (Oxford University Press, 2007). https://doi.org/10.1093/acprof:oso/9780199208784.003.0015.Berger, J. & Gompper, M. E. Sex ratios in extant ungulates: products of contemporary predation or past life histories? J. Mammal. 80, 1084–1113 (1999).
    Google Scholar 
    Christe, P., Keller, L. & Roulin, A. The predation cost of being a male: implications for sex-specific rates of ageing. Oikos 114, 381–384 (2006).
    Google Scholar 
    Boukal, D. S., Berec, L. & Křivan, V. Does sex-selective predation stabilize or destabilize predator-prey dynamics? PLoS ONE 3, e2687 (2008).PubMed 
    PubMed Central 

    Google Scholar 
    Moore, S. L. & Wilson, K. Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297, 2015–2018 (2002).PubMed 

    Google Scholar 
    Fairbairn, D., Blanckenhorn, W. & Székely, T. Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism. Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism https://doi.org/10.1093/acprof:oso/9780199208784.001.0001 (2007).Székely, T., Liker, A., Freckleton, R. P., Fichtel, C. & Kappeler, P. M. Sex-biased survival predicts adult sex ratio variation in wild birds. Proc. R. Soc. B: Biol. Sci. 281, 20140342 (2014).
    Google Scholar 
    Tidière, M. et al. Does sexual selection shape sex differences in longevity and senescence patterns across vertebrates? A review and new insights from captive ruminants. Evolution 69, 3123–3140 (2015).PubMed 

    Google Scholar 
    Lemaître, J.-F. et al. Sex differences in adult lifespan and aging rates of mortality across wild mammals. Proc. Natl Acad. Sci. USA 117, 8546–8553 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    Wedekind, C. et al. Persistent unequal sex ratio in a population of grayling (Salmonidae) and possible role of temperature increase. Conserv. Biol. 27, 229–234 (2013).PubMed 

    Google Scholar 
    Eberhart-Phillips, L. J. et al. Demographic causes of adult sex ratio variation and their consequences for parental cooperation. Nat. Commun. 9, 1651 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    Schacht, R., Macfarlan, S. J., Meeks, H., Cervantes, P. L. & Morales, F. Male survival advantage on the Baja California peninsula. Biol. Lett. 16, 20200600 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    Schacht, R., Tharp, D. & Smith, K. R. Sex ratios at birth vary with environmental harshness but not maternal condition. Sci. Rep. 9, 9066 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    Schacht, R. et al. Frail males on the American frontier: the role of environmental harshness on sex ratios at birth across a period of rapid industrialization. Soc. Sci. 10, 319 (2021).
    Google Scholar 
    Casey, J. A., Gemmill, A., Elser, H., Karasek, D. & Catalano, R. Sun smoke in Sweden: perinatal implications of the Laki volcanic eruptions, 1783–1784. Epidemiology 30, 330–333 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    Catalano, R., Bruckner, T. & Smith, K. R. Ambient temperature predicts sex ratios and male longevity. Proc. Natl Acad. Sci. USA 105, 2244–2247 (2008).PubMed 
    PubMed Central 

    Google Scholar 
    Hollingshaus, M., Utz, R., Schacht, R. & Smith, K. R. Sex ratios and life tables: Historical demography of the age at which women outnumber men in seven countries, 1850–2016. Historical Methods.: A J. Quant. Interdiscip. Hist. 52, 244–253 (2019).
    Google Scholar 
    Li, X.-Y. & Kokko, H. Sex-biased dispersal: a review of the theory. Biol. Rev. 94, 721–736 (2019).PubMed 

    Google Scholar 
    Alho, J. S., Matsuba, C. & Merilä, J. Sex reversal and primary sex ratios in the common frog (Rana temporaria). Mol. Ecol. 19, 1763–1773 (2010).PubMed 

    Google Scholar 
    Sandercock, B. K., Beissinger, S. R., Stoleson, S. H., Melland, R. R. & Hughes, C. R. Survival rates of a neotropical parrot: implications for latitudinal comparisons of avian demography. Ecology 81, 1351–1370 (2000).Budden, A. E. & Beissinger, S. R. Against the odds? Nestling sex ratio variation in green-rumped parrotlets. Behav. Ecol. 15, 607–613 (2004).
    Google Scholar 
    Thompson, F. J. et al. Reproductive competition triggers mass eviction in cooperative banded mongooses. Proc. Biol. Sci. 283, 20152607 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Jaccarini, V., AGius, L., Schembri, P. J. & Rizzo, M. Sex determination and larval sexual interaction in Bonellia viridis Rolando (Echiura: Bonelliidae). J. Exp. Mar. Biol. Ecol. 66, 25–40 (1983).
    Google Scholar 
    Tingley, G. & Anderson, R. Environmental sex determination and density-dependent population regulation in the entomogenous nematode Romanomermis culcivorax. Parasitology 92, 431–449 (1986).
    Google Scholar 
    Hardisty, M. W. Sex composition of lamprey populations. Nature 191, 1116–1117 (1961).
    Google Scholar 
    Docker, M. F., William, F. & Beamish, H. Age, growth, and sex ratio among populations of least brook lamprey, Lampetra aepyptera, larvae: an argument for environmental sex determination. Environ. Biol. Fish. 41, 191–205 (1994).
    Google Scholar 
    Geffroy, B. & Bardonnet, A. Sex differentiation and sex determination in eels: consequences for management. Fish. Fish. 17, 375–398 (2016).
    Google Scholar 
    Ribas, L., Valdivieso, A., Díaz, N. & Piferrer, F. Appropriate rearing density in domesticated zebrafish to avoid masculinization: links with the stress response. J. Exp. Biol. 220, 1056–1064 (2017).PubMed 

    Google Scholar 
    García-Cruz, E. L. et al. Crowding stress during the period of sex determination causes masculinization in pejerrey Odontesthes bonariensis, a fish with temperature-dependent sex determination. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 245, 110701 (2020).PubMed 

    Google Scholar 
    Geffroy, B. et al. Parental selection for growth and early-life low stocking density increase the female-to-male ratio in European sea bass. Sci. Rep. 11, 13620 (2021).PubMed 
    PubMed Central 

    Google Scholar 
    Fricke, H. & Fricke, S. Monogamy and sex change by aggressive dominance in coral reef fish. Nature 266, 830–832 (1977).PubMed 

    Google Scholar 
    Todd, E. V. et al. Stress, novel sex genes, and epigenetic reprogramming orchestrate socially controlled sex change. Sci. Adv. 5, eaaw7006 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    Kuwamura, T., Nakashimn, Y. & Yogo, Y. Sex change in either direction by growth-rate advantage in the monogamous coral goby, Paragobiodon echinocephalus. Behav. Ecol. 5, 434–438 (1994).
    Google Scholar 
    Rodgers, E. W., Earley, R. L. & Grober, M. S. Social status determines sexual phenotype in the bi-directional sex changing bluebanded goby Lythrypnus dalli. J. Fish. Biol. 70, 1660–1668 (2007).
    Google Scholar 
    Munday, P. L., Caley, M. J. & Jones, G. P. Bi-directional sex change in a coral-dwelling goby. Behav. Ecol. Sociobiol. 43, 371–377 (1998).
    Google Scholar 
    Goikoetxea, A., Todd, E. V. & Gemmell, N. J. Stress and sex: does cortisol mediate sex change in fish? Reproduction 154, R149–R160 (2017).PubMed 

    Google Scholar 
    Nozu, R. & Nakamura, M. Cortisol administration induces sex change from ovary to testis in the protogynous Wrasse, Halichoeres trimaculatus. Sex. Dev. 9, 118–124 (2015).PubMed 

    Google Scholar 
    Olivotto, I. & Geffroy, B. Clownfish. in Marine Ornamental Species Aquaculture (eds. Calado, R., Olivotto, I., Oliver, M. P. & Holt, G. J.) 177–199 (John Wiley & Sons, Ltd, 2017). https://doi.org/10.1002/9781119169147.ch12.Bessa, E., Brandão, M. L. & Gonçalves-de-Freitas, E. Integrative approach on the diversity of nesting behaviour in fishes. Fish Fisheries 23, 564–583 (2022).Safari, I. & Goymann, W. The evolution of reversed sex roles and classical polyandry: Insights from coucals and other animals. Ethology 127, 1–13 (2021).
    Google Scholar 
    Komdeur, J., Székely, T., Long, X. & Kingma, S. A. Adult sex ratios and their implications for cooperative breeding in birds. Philos. Trans. R. Soc. Lond. B Biol. Sci. 372, 20160322 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Jankowiak, Ł., Tryjanowski, P., Hetmański, T. & Skórka, P. Experimentally evoked same-sex sexual behaviour in pigeons: better to be in a female-female pair than alone. Sci. Rep. 8, 1654 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    Darwin, C. The Descent of Man, and Selection in Relation to Sex (John Murray, 1871).Bleu, J., Bessa-Gomes, C. & Laloi, D. Evolution of female choosiness and mating frequency: effects of mating cost, density and sex ratio. Anim. Behav. 83, 131–136 (2012).
    Google Scholar 
    Forsgren, E., Amundsen, T., Borg, A. A. & Bjelvenmark, J. Unusually dynamic sex roles in a fish. Nature 429, 551–554 (2004).PubMed 

    Google Scholar 
    Monier, M., Nöbel, S., Isabel, G. & Danchin, E. Effects of a sex ratio gradient on female mate-copying and choosiness in Drosophila melanogaster. Curr. Zool. 64, 251–258 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    Jirotkul, M. Operational sex ratio influences preference and male–male competition in guppies. Anim. Behav. 58, 287–294 (1999).PubMed 

    Google Scholar 
    Grant, P. R. & Grant, B. R. Adult sex ratio influences mate choice in Darwin’s finches. Proc. Natl Acad. Sci. USA 116, 12373–12382 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    Queller, D. C. Why do females care more than males? Proc. Biol. Sci. 264, 1555–1557 (1997). A prescient overview that explains why females are more likely than males to provide care, including the explanation that a female-biased ASR means that males have a higher mean mating rate than females, which makes caring more costly for males.PubMed Central 

    Google Scholar 
    Janicke, T., Häderer, I. K., Lajeunesse, M. J. & Anthes, N. Darwinian sex roles confirmed across the animal kingdom. Sci. Adv. 2, e1500983 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Liker, A. et al. Evolution of large males is associated with female‐skewed adult sex ratios in amniotes. Evolution 75, 1636–1649 (2021).PubMed 

    Google Scholar 
    Clutton-Brock, T. H., Harvey, P. H. & Rudder, B. Sexual dimorphism, socionomic sex ratio and body weight in primates. Nature 269, 797–800 (1977).PubMed 

    Google Scholar 
    Wittenberger, J. F. The evolution of mating systems in grouse. Condor 80, 126–137 (1978).
    Google Scholar 
    Vahl, W. K., Boiteau, G., Heij, M. E., de, MacKinley, P. D. & Kokko, H. Female fertilization: effects of sex-specific density and sex ratio determined experimentally for colorado potato beetles and drosophila fruit flies. PLoS ONE 8, e60381 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    House, C. M., Rapkin, J., Hunt, J. & Hosken, D. J. Operational sex ratio and density predict the potential for sexual selection in the broad-horned beetle. Anim. Behav. 152, 63–69 (2019).
    Google Scholar 
    Warner, R. R. & Hoffman, S. G. Population density and the economics of territorial defense in a coral reef fish. Ecology 61, 772–780 (1980).
    Google Scholar 
    Pröhl, H. Population differences in female resource abundance, adult sex ratio, and male mating success in Dendrobates pumilio. Behav. Ecol. 13, 175–181 (2002).
    Google Scholar 
    McNamara, J. M., Székely, T., Webb, J. N. & Houston, A. I. A dynamic game-theoretic model of parental care. J. Theor. Biol. 205, 605–623 (2000).PubMed 

    Google Scholar 
    Davies, N. B. Dunnock Behaviour and Social Evolution. (Oxford University Press, 1992).Pilastro, A., Biddau, L., Marin, G. & Mingozzi, T. Female brood desertion increases with number of available mates in the Rock Sparrow. J. Avian Biol. 32, 68–72 (2001).
    Google Scholar 
    Rossmanith, E., Grimm, V., Blaum, N. & Jeltsch, F. Behavioural flexibility in the mating system buffers population extinction: lessons from the lesser spotted woodpecker Picoides minor. J. Anim. Ecol. 75, 540–548 (2006).PubMed 

    Google Scholar 
    Liker, A., Freckleton, R. P. & Székely, T. The evolution of sex roles in birds is related to adult sex ratio. Nat. Commun. 4, 1587 (2013). An important comparative study that shows both social mating system and parenting are associated with ASR in shorebirds.PubMed 

    Google Scholar 
    Liker, A., Freckleton, R. P. & Székely, T. Divorce and infidelity are associated with skewed adult sex ratios in birds. Curr. Biol. 24, 880–884 (2014).PubMed 

    Google Scholar 
    Balshine-Earn, S. & Earn, D. J. D. On the evolutionary pathway of parental care in mouth-brooding cichlid fishes. Proc. ofn R. Soc. 265, 2217–2222 (1998).
    Google Scholar 
    Parra, J. E., Beltrán, M., Zefania, S., Dos Remedios, N. & Székely, T. Experimental assessment of mating opportunities in three shorebird species. Anim. Behav. 90, 83–90 (2014).
    Google Scholar 
    Székely, T., Cuthill, I. & Kis, J. Brood desertion in Kentish plover: sex differences in remating opportunities. Behav. Ecol. 10, 185–190 (1999). An important early field study showing that intraspecific variation in parental care can be explained by the availability of mates, which in turn depends on the prevailing ASR.
    Google Scholar 
    Clutton-Brock, T. H. The Evolution of Parental Care. The Evolution of Parental Care (Princeton University Press, 1991). https://doi.org/10.1515/9780691206981.Bessa-Gomes, C., Legendre, S. & Clobert, J. Allee effects, mating systems and the extinction risk in populations with two sexes. Ecol. Lett. 7, 802–812 (2004).
    Google Scholar 
    Lindström, J. & Kokko, H. Sexual reproduction and population dynamics: the role of polygyny and demographic sex differences. Proc. Biol. Sci. 265, 483–488 (1998).PubMed 
    PubMed Central 

    Google Scholar 
    Lee, A. M., Saether, B.-E. & Engen, S. Demographic stochasticity, allee effects, and extinction: the influence of mating system and sex ratio. Am. Naturalist 177, 301–313 (2011).
    Google Scholar 
    Leach, D., Shaw, A. K. & Weiss-Lehman, C. Stochasticity in social structure and mating system drive extinction risk. Ecosphere 11, e03038 (2020).
    Google Scholar 
    Gownaris, N. J. & Boersma, P. D. Sex-biased survival contributes to population decline in a long-lived seabird, the Magellanic Penguin. Ecol. Appl. 29, 1–17 (2019).
    Google Scholar 
    Le Galliard, J.-F., Fitze, P. S., Ferrière, R. & Clobert, J. Sex ratio bias, male aggression, and population collapse in lizards. Proc. Natl Acad. Sci. USA 102, 18231–18236 (2005).PubMed 
    PubMed Central 

    Google Scholar 
    Lea, J. M. D. et al. Non-invasive physiological markers demonstrate link between habitat quality, adult sex ratio and poor population growth rate in a vulnerable species, the Cape mountain zebra. Funct. Ecol. 32, 300–312 (2018).
    Google Scholar 
    Dreiss, A. N., Cote, J., Richard, M., Federici, P. & Clobert, J. Age-and sex-specific response to population density and sex ratio. Behav. Ecol. 21, 356–364 (2010).
    Google Scholar 
    Dale, S. Female-biased dispersal, low female recruitment, unpaired males, and the extinction of small and isolated bird populations. Oikos 92, 344–356 (2001).
    Google Scholar 
    Morrison, C. A., Robinson, R. A., Clark, J. A. & Gill, J. A. Causes and consequences of spatial variation in sex ratios in a declining bird species. J. Anim. Ecol. 85, 1298–1306 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Chipman, A. & Morrison, E. The impact of sex ratio and economic status on local birth rates. Biol. Lett. 9, 20130027 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    Krainacker, D. A. & Carey, J. R. Sex ratio in a wild population of twospotted spider mites. Holarct. Ecol. 14, 97–103 (1991).
    Google Scholar 
    Bunnell, D. B., Madenjian, C. P. & Croley, T. E. Long-term trends of bloater (Coregonus hoyi) recruitment in Lake Michigan: evidence for the effect of sex ratio. Can. J. Fish. Aquat. Sci. 63, 832–844 (2006).
    Google Scholar 
    Forbes, M. R., McCurdy, D. G., Lui, K., Mautner, S. I. & Boates, J. S. Evidence for seasonal mate limitation in populations of an intertidal amphipod, Corophium volutator (Pallas). Behav. Ecol. Sociobiol. 60, 87–95 (2006).
    Google Scholar 
    Solberg, E. J., Loison, A., Ringsby, T. H., Sæther, B. E. & Heim, M. Biased adult sex ratio can affect fecundity in primiparous moose Alces alces. Wildl. Biol. 8, 117–128 (2002).
    Google Scholar 
    Pipoly, I., Székely, T. & Liker, A. Multiple paternity is related to adult sex ratio and sex determination system in reptiles. Journal of Evolutionary Biology (under review).Jones, A. G., Rosenqvist, G., Berglund, A., Arnold, S. J. & Avise, J. C. The Bateman gradient and the cause of sexual selection in a sex–role–reversed pipefish. Proc. R. Soc. Lond. Ser. B: Biol. Sci. 267, 677–680 (2000).
    Google Scholar 
    Clutton-Brock, T. H., Coulson, T. N., Milner-Gulland, E. J., Thomson, D. & Armstrong, H. M. Sex differences in emigration and mortality affect optimal management of deer populations. Nature 415, 633–637 (2002).PubMed 

    Google Scholar 
    Lambertucci, S. A., Carrete, M., Speziale, K. L., Hiraldo, F. & Donázar, J. A. Population sex ratios: another consideration in the reintroduction – reinforcement debate? PLoS ONE 8, e75821 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    Snyder, K. T., Freidenfelds, N. A. & Miller, T. E. X. Consequences of sex-selective harvesting and harvest refuges in experimental meta-populations. Oikos 123, 309–314 (2014).
    Google Scholar 
    Frankham, R. Effective population size/adult population size ratios in wildlife: a review. Genet. Res. 66, 95–107 (1995).
    Google Scholar 
    Sæther, B.-E. et al. Time to extinction in relation to mating system and type of density regulation in populations with two sexes. J. Anim. Ecol. 73, 925–934 (2004).
    Google Scholar 
    Milner, J., Nilsen, E. & Andreassen, H. Demographic side effects of selective hunting in ungulates and carnivores. Conserv. Biol.: J. Soc. Conserv. Biol. 21, 36–47 (2007).
    Google Scholar 
    Heinsohn, R., Olah, G., Webb, M., Peakall, R. & Stojanovic, D. Sex ratio bias and shared paternity reduce individual fitness and population viability in a critically endangered parrot. J. Anim. Ecol. 88, 502–510 (2019).PubMed 

    Google Scholar 
    Lee, P. L. M., Schofield, G., Haughey, R. I., Mazaris, A. D. & Hays, G. C. A review of patterns of multiple paternity across sea turtle rookeries. Adv. Mar. Biol. 79, 1–31 (2018).PubMed 

    Google Scholar 
    Wayne, A. F. et al. Sudden and rapid decline of the abundant marsupial Bettongia penicillata in Australia. Oryx 49, 175–185 (2015).
    Google Scholar 
    Roscoe, P. Dead Birds: The “Theater” of War among the Dugum Dani. Am. Anthropologist 113, 56–70 (2011).
    Google Scholar 
    Bethmann, D. & Kvasnicka, M. World war ii, missing men and out of wedlock childbearing. Economic J. 123, 162–194 (2013).
    Google Scholar 
    Schradin, C. et al. Geographic intra-specific variation in social organization is driven by population density. Behav. Ecol. Sociobiol. 74, (2020).Brandner, J. L., Dillon, H. M. & Brase, G. L. Convergent evidence for a theory of rapid, automatic, and accurate sex ratio tracking. Acta Psychologica 210, (2020).Griskevicius, V. et al. The financial consequences of too many men: sex ratio effects on saving, borrowing, and spending. J. Personal. Soc. Psychol. 102, 69–80 (2011).
    Google Scholar 
    Fritzsche, K., Booksmythe, I. & Arnqvist, G. Sex ratio bias leads to the evolution of sex role reversal in honey locust beetles. Curr. Biol. 26, 2522–2526 (2016).PubMed 

    Google Scholar 
    Bath, E. et al. Sex ratio and the evolution of aggression in fruit flies. Proc. R. Soc. B: Biol. Sci. 288, 20203053 (2021).
    Google Scholar 
    Beltran, S., Cézilly, F. & Boissier, J. Adult sex ratio affects divorce rate in the monogamous endoparasite Schistosoma mansoni. Behav. Ecol. Sociobiol. 63, 1363–1368 (2009).
    Google Scholar 
    Chuard, P., Brown, G. & Grant, J. The effects of adult sex ratio on mating competition in male and female guppies (Poecilia reticulata) in two wild populations. Behavioural Process. 129, 1–10 (2016).
    Google Scholar 
    Lande, R. Risks of population extinction from demographic and environmental stochasticity and random catastrophes. Am. Naturalist 142, 911–927 (1993).
    Google Scholar 
    May, R. & Allen, P. Stability and complexity in model ecosystems. Syst., Man Cybern., IEEE Trans. 44, 887–887 (1977).
    Google Scholar 
    Wobst, H. M. Boundary conditions for paleolithic social systems: a simulation approach. Am. Antiquity 39, 147–178 (1974).
    Google Scholar 
    Dyson, T. Causes and Consequences of Skewed Sex Ratios. (2012) https://doi.org/10.1146/annurev-soc-071811-145429.Edlund, L. Son preference, sex ratios, and marriage patterns. J. Political Econ. 107, 1275–1304 (1999).
    Google Scholar 
    Hesketh, T. & Xing, Z. W. Abnormal sex ratios in human populations: causes and consequences. Proc. Natl Acad. Sci. USA 103, 13271–13275 (2006).PubMed 
    PubMed Central 

    Google Scholar 
    Hesketh, T. & Min, J. M. The effects of artificial gender imbalance. EMBO Rep. 13, 487–492 (2012).PubMed 
    PubMed Central 

    Google Scholar 
    Schacht, R. & Kramer, K. L. Patterns of family formation in response to sex ratio variation. PLoS ONE 11, e0160320 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Schacht, R., Tharp, D. & Smith, K. R. Marriage markets and male mating effort: violence and crime are elevated where men are rare. Hum. Nat. 27, 489–500 (2016).PubMed 

    Google Scholar 
    Pouget, E. R. Social determinants of adult sex ratios and racial/ethnic disparities in transmission of HIV and other sexually transmitted infections in the USA. Philos. Trans. R. Soc. Lond. B Biol. Sci. 372, 20160323 (2017). An important study on humans that bridges the gap between theory and policy illustrating a societal issue related to sex ratio imbalance and sexually transmitted diseases risk in a vulnerable sub-population in the USA.PubMed 
    PubMed Central 

    Google Scholar 
    Del Giudice, M. Sex ratio dynamics and fluctuating selection on personality. J. Theor. Biol. 297, 48–60 (2012).PubMed 

    Google Scholar 
    Schacht, R. & Borgerhoff Mulder, M. Sex ratio effects on reproductive strategies in humans. R. Soc. Open Sci. 2, 140402 (2015). A pioneering study of a small-scale population that demonstrates mating strategies vary with the sex ratio at local level.PubMed 
    PubMed Central 

    Google Scholar 
    Jones, J. H. & Ferguson, B. Demographic and Social predictors of intimate partner violence in colombia: a dyadic power perspective. Hum. Nat. 20, 184–203 (2009).PubMed 

    Google Scholar 
    Uggla, C. & Mace, R. Local ecology influences reproductive timing in Northern Ireland independently of individual wealth. Behav. Ecol. 27, 158–165 (2016).
    Google Scholar 
    Guttentag, M. & Secord, P. Too Many Women? SAGE Publications Inc (1983). A landmark book that presented historical and quantitative evidence for how sex ratio skew impacts family structure and the societal values applied to men and women.United Nations Population Fund Annual Report. https://www.unfpa.org/annual-report-2020 (2020)Schmitt, D. P. Sociosexuality from Argentina to Zimbabwe: a 48-nation study of sex, culture, and strategies of human mating. Behav. Brain Sci. 28, 247–275 (2005).PubMed 

    Google Scholar 
    Baumeister, R. F. & Vohs, K. D. Sexual economics: sex as female resource for social exchange in heterosexual interactions. Pers. Soc. Psychol. Rev. 8, 339–363 (2004).PubMed 

    Google Scholar 
    Reid, P. C. et al. Global impacts of the 1980s regime shift. Glob. Change Biol. 22, 682–703 (2016).
    Google Scholar 
    Grafe, T. U. & Linsenmair, K. E. Protogynous sex change in the reed frog Hyperolius viridiflavus. Copeia 1989, 1024–1029 (1989).
    Google Scholar 
    Trochet, A. et al. Population sex ratio and dispersal in experimental, two-patch metapopulations of butterflies. J. Anim. Ecol. 82, 946–955 (2013).PubMed 

    Google Scholar 
    Thomson, D., Cooch, E. & Conroy, M. Modeling demographic processes in marked populations. https://doi.org/10.1007/978-0-387-78151-8 (2009).Dail, D. & Madsen, L. Models for estimating abundance from repeated counts of an open metapopulation. Biometrics 67, 577–587 (2011).PubMed 

    Google Scholar 
    Kéry, M. & Royle, J. Andrew. Applied Hierarchical Modeling in Ecology: Analysis of distribution, abundance and species richness in R and BUGS. 783 (2015).US Census Bureau. Accuracy and coverage evaluation of Census 2000: Design and Methodology. (2004).Guillot, M. The dynamics of the population sex ratio in India, 1971-96. Popul. Stud. 56, 51–63 (2002).
    Google Scholar 
    Dyson, E. A. & Hurst, G. D. D. Persistence of an extreme sex-ratio bias in a natural population. Proc. Natl Acad. Sci. USA 101, 6520–6523 (2004).PubMed 
    PubMed Central 

    Google Scholar 
    Hays, G. C., Mazaris, A. D., Schofield, G. & Laloë, J.-O. Population viability at extreme sex-ratio skews produced by temperature-dependent sex determination. Proc. R. Soc. B. 284, 20162576 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Rózsa, L., Reiczigel, J. & Majoros, G. Quantifying parasites in samples of hosts. J. Parasitol. 86, 228–232 (2000).PubMed 

    Google Scholar 
    Cockburn, A., Scott, M. P. & Dickman, C. R. Sex ratio and intrasexual kin competition in mammals. Oecologia 66, 427–429 (1985).PubMed 

    Google Scholar 
    Douglas III, H. & Malenke, J. R. An Extraordinary Host-Specific Sex Ratio in an Avian Louse (Phthiraptera: Insecta)-Chemical Distortion? Environ. Entomol. (2015).Bonnet, X. et al. A prison effect in a wild population: a scarcity of females induces homosexual behaviors in males. Behav. Ecol. 27, 1206–1215 (2016).
    Google Scholar 
    Beltran, S. & Boissier, J. Male-biased sex ratio: why and what consequences for the genus Schistosoma? Trends Parasitol. 26, 63–69 (2010).PubMed 

    Google Scholar 
    Beltran, S. & Boissier, J. Schistosome monogamy: who, how, and why? Trends Parasitol. 24, 386–391 (2008).PubMed 

    Google Scholar 
    Fisher, R. The Genetical Theory of Natural Selection (The Clarendon Press, 1930).Houston, A. & McNamara, J. John Maynard Smith and the importance of consistency in evolutionary game theory. Biol. Philos. 20, 933–950 (2005).
    Google Scholar 
    Kokko, H. & Jennions, M. D. Sex differences in parental care. in The Evolution of Parental Care (Oxford University Press, 2012). https://doi.org/10.1093/acprof:oso/9780199692576.003.0006.Fromhage, L. & Jennions, M. D. Coevolution of parental investment and sexually selected traits drives sex-role divergence. Nat. Commun. 7, 12517 (2016). A theoretical study showing that under a simple null scenario the sex ratio of male to female care does not evolve in response to ASR, but rather to the sex ratio at maturation.PubMed 
    PubMed Central 

    Google Scholar 
    Long, X. The Evolution of Parental Sex Roles. PhD dissertation, University of Groningen (2020).Seger, J. & Stubblefield, J. W. Models of sex ratio evolution. in Sex Ratios: Concepts and Research Methods (ed. Hardy, I. C. W.) 2–25 (Cambridge University Press, 2002). https://doi.org/10.1017/CBO9780511542053.002.Pen, I. & Weissing, F. J. Optimal sex allocation: steps towards a mechanistic theory. in Sex Ratios: Concepts and Research Methods (ed. Hardy, I. C. W.) 26–46 (Cambridge University Press, 2002). https://doi.org/10.1017/CBO9780511542053.003.Bodmer, W. & Edwards, A. Natural selection and the sex ratio. Ann. Hum. Genet. 239–244, (1960).Sampson, R. J., Laub, J. H. & Wimer, C. Does marriage reduce crime? A counterfactual approach to within-individual causal effects. Criminology 44, 465–508 (2006).
    Google Scholar 
    Avakame, E. F. Sex ratios, female labor force participation, and lethal violence against women: extending Guttentag and Secord’s Thesis. Violence Women 5, 1321–1341 (1999).
    Google Scholar 
    Diamond-Smith, N. & Rudolph, K. The association between uneven sex ratios and violence: Evidence from 6 Asian countries. PLoS ONE 13, e0197516 (2018). One of the few studies on crime and sex ratios that uses individual-level data of reported crime as linked to area level sex ratio skew.PubMed 
    PubMed Central 

    Google Scholar 
    Drèze, J. & Khera, R. Crime, gender, and society in India: Insights from homicide data. Popul. Dev. Rev. 26, 335–352 (2000).PubMed 

    Google Scholar 
    Edlund, L., Li, H., Yi, J. & Zhang, J. Sex ratios and crime: evidence from China. Rev. Econ. Stat. 95, 1520–1534 (2013).
    Google Scholar 
    Messner, S. F. & Sampson, R. J. The sex ratio, family disruption, and rates of violent crime: the paradox of demographic structure. Soc. Forces 69, 693–713 (1991).
    Google Scholar 
    Trent, K. & South, S. J. Mate availability and women’s sexual experiences in China. J. Marriage Fam. 74, 201–214 (2012).PubMed 
    PubMed Central 

    Google Scholar 
    Filser, A., Barclay, K., Beckley, A., Uggla, C. & Schnettler, S. Are skewed sex ratios associated with violent crime? A longitudinal analysis using Swedish register data. Evolution Hum. Behav. 42, 212–222 (2021).
    Google Scholar 
    Barber, N. The sex ratio as a predictor of cross-national variation in violent crime. Cross-Cultural Res. 34, 264–282 (2000).
    Google Scholar 
    Barber, N. Countries with fewer males have more violent crime: marriage markets and mating aggression. Aggress. Behav. 35, 49–56 (2009).PubMed 

    Google Scholar 
    Obrien, R. M. Sex ratios and rape rates: a powercontrol theory. Criminology 29, 99–114 (1991).
    Google Scholar 
    Esmail, A. M., Penny, J. & Eargle, L. A. The impact of culture on crime. Race Gender Class 20, 326–343 (2013).
    Google Scholar 
    Pollet, T. V., Stoevenbelt, A. H. & Kuppens, T. The potential pitfalls of studying adult sex ratios at aggregate levels in humans. Philos. Trans. R. Soc. B: Biol. Sci. 372, (2017). A critical study that highlights shortcomings inherent in much of the early sex ratio literature, which stems in part from using nation- rather than local-level data.Uggla, C. & Mace, R. Adult sex ratio and social status predict mating and parenting strategies in Northern Ireland. Philos. Trans. R. Soc. B: Biol. Sci. 372, 20160318 (2017). A seminal study on humans demonstrating the impacts of local sex ratio skew depending on individual status on the mating market.
    Google Scholar 
    Schacht, R. & Uggla, C. Beyond sex: reproductive strategies as a function of local sex ratio variation. in The Oxford Handbook of Human Mating (Oxford University Press, 2022). More

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    Tube length of chironomid larvae as an indicator for dissolved oxygen in water bodies

    Chironomids have the ability to survive and reproduce in polluted environments, and thus they are included in many ecological studies where approaches may be taxonomic or functional16. The diversity of most macroinvertebrates is controlled by the oxygen level of water, but chironomids may survive in hypoxic conditions where the oxygen concentration may be less than 3 mg l−117. The current study demonstrates that changing seasons, as well as anthropogenic activities, have a significant impact on the levels of DO in aquatic bodies. As observed from the result, DO highly influences the tube length of the chironomid larvae. Since KWC is a wastewater canal, the average oxygen level is lower (5.24 ± 1.14 mg l−1) than KFP (6.63 ± 1.28 mg l−1) which is a normal fish culturing pond. It has also been observed that the average tube length of the chironomid larvae of KWC (8.66 ± 0.88 mm) is higher than KFP (7.68 ± 0.62 mm), which indicates that a low concentration of DO promotes the building of longer tubes in natural conditions. Similar observations were also observed in laboratory conditions. When the oxygen level (7.03 ± 0.41 mg l−1) in the experiment was kept in the normal range, there was negligible variation in tube length (7.61 ± 0.31 mm). But when the concentration of oxygen is gradually reduced by dilution, the tube length starts to increase accordingly, which is explained graphically in Fig. 4. The regression model of both the experimental conditions also supports the hypothesis that the tube length has an inverse relationship with DO. The scatter plot and simple linear regression confirmed the inverse relationship between DO and tube length (Figs. 1 and 2).Chironomid larvae are able to grow in the polluted water of a wastewater pond as dominant macroinvertebrates18. It is observed that those larvae living in the sand tubes are more susceptible to chemical pollutants than the larvae living in silt tubes7. Sand particles are bigger than silt and are not suitable for the survival of larvae19. Chironomus riparius larvae make their tubes from different external particles and their own proteins20. Midge larvae are the inhabitants of sediments, and at the same time, sediment is the depository of different inorganic, organic, and heavy metals. In such cases, the tube of chironomid larvae may act as a defensive structure, which protects them from the adverse effects of undesirable pollutants and may increase their tolerance against such chemicals21,22,23.Larvae can thrive in benthic sediments with high decaying organic content and very low DO concentrations in water bodies24. In poor DO concentration, larvae can survive due to the presence of haemoglobin in their body tissue fluid, which plays an important physiological role in increasing respiratory efficiency, as was observed in Chironomus plumosus. Longer tube length may help larvae generate better respiratory currents so that they can cope with a low DO environment.Tube length is crucial for living in water because primarily tubes protect them from outer environmental factors like predators, and pollution. It was observed during this study that when the DO of water is low, larvae make elongated tubes to reach the upper layer of water, where the DO level is comparatively high. To get their required amount of oxygen, the larvae increase the tube length towards the water surface and increase the DO in tube water by undulating the body and other structures, creating a current inside the tube25,26. On contrary, when the DO level of the surrounding water of chironomid is sufficient, they can manage their normal physiological activities with the available oxygen. They need not to elongate their tube length. That’s why their tube length is inversely related to the DO of their surrounding medium.If tube length does not increase in size in hypoxic water, larvae will not be able to meet their oxygen demand. If the DO of water decreases, tube length will increase and vice versa. Behavioural and physiological adaptations of chironomids larvae make them successful to live in a hypoxic environment. Thus, in hypoxic conditions, larvae with longer tubes are able to gather more oxygen from the upper layer of water and get more space to create a current of water to increase the amount of O2 inside the tube by undulating the preanal papillae, anal gill, ventral gills. This would explain why the tube length of chironomids depends on the DO of water. Hence by measuring the tube length with a standard measuring scale, one may get an idea about the quality of water, especially DO, before doing any chemical analysis. The work seems to be unique and novel for its own kind. More

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    Influence of short and long term processes on SAR11 communities in open ocean and coastal systems

    Thrash JC, Boyd A, Huggett MJ, Grote J, Carini P, Yoder RJ, et al. Phylogenomic evidence for a common ancestor of mitochondria and the SAR11 clade. Sci Rep. 2011;1:9.
    Google Scholar 
    Ferla MP, Thrash JC, Giovannoni SJ, Patrick WM. New rRNA gene-based phylogenies of the alphaproteobacteria provide perspective on major groups, mitochondrial ancestry and phylogenetic instability. PLoS One. 2013;8:e83383.
    Google Scholar 
    Giovannoni SJ. SAR11 bacteria: the most abundant plankton in the oceans. Annu Rev Mar Sci. 2017;9:231–55.
    Google Scholar 
    Zhao X, Schwartz CL, Pierson J, Giovannoni SJ, McIntosh RJ, Nicastro D. Three-dimensional structure of the ultraoligotrophic marine bacterium “Candidatus pelagibacter ubique”. Appl Environ Microbiol. 2017;83:807–16.
    Google Scholar 
    Giovannoni SJ, DeLong EF, Schmidt TM, Pace NR. Tangential flow filtration and preliminary phylogenetic analysis of marine picoplankton. Appl Environ Microbiol. 1990;56:4.
    Google Scholar 
    Morris RM, Rappé MS, Connon SA, Vergin KL, Siebold WA, Carlson CA, et al. SAR11 clade dominates ocean surface bacterioplankton communities. Nature. 2002;420:806–10.CAS 

    Google Scholar 
    Rappé MS, Connon SA, Vergin KL, Giovannoni SJ. Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature. 2002;418:630–3.
    Google Scholar 
    Grote J, Thrash JC, Huggett MJ, Landry ZC, Carini P, Giovannoni SJ, et al. Streamlining and core genome conservation among highly divergent members of the SAR11 clade. mBio. 2012;3:e00252–12.CAS 

    Google Scholar 
    Field KG, Gordon D, Wright T, Rappé M, Urback E, Vergin K, et al. Diversity and depth-specific distribution of SAR11 cluster rRNA genes from marine planktonic bacteria. Appl Environ Microbiol. 1997;63:63–70.CAS 

    Google Scholar 
    Suzuki MT, Beja O, Taylor LT, DeLong EF. Phylogenetic analysis of ribosomal RNA operons from uncultivated coastal marine bacterioplankton. Environ Microbiol. 2001;3:323–31.CAS 

    Google Scholar 
    Carlson CA, Morris R, Parsons R, Treusch AH, Giovannoni SJ, Vergin K. Seasonal dynamics of SAR11 populations in the euphotic and mesopelagic zones of the northwestern Sargasso Sea. ISME J. 2009;3:283–95.CAS 

    Google Scholar 
    Brown MV, Lauro FM, DeMaere MZ, Muir L, Wilkins D, Thomas T, et al. Global biogeography of SAR11 marine bacteria. Mol Syst Biol. 2012;8:595.
    Google Scholar 
    Haro‐Moreno JM, Rodriguez‐Valera F, Rosselli R, Martinez‐Hernandez F, Roda‐Garcia JJ, Gomez ML, et al. Ecogenomics of the SAR11 clade. Environ Microbiol. 2020;22:1748–63.
    Google Scholar 
    Carini P, White AE, Campbell EO, Giovannoni SJ. Methane production by phosphate-starved SAR11 chemoheterotrophic marine bacteria. Nat Commun. 2014;5:4346.CAS 

    Google Scholar 
    Sun J, Steindler L, Thrash JC, Halsey KH, Smith DP, Carter AE, et al. One carbon metabolism in SAR11 Pelagic marine bacteria. PLoS One. 2011;6:e23973.CAS 

    Google Scholar 
    Schwalbach MS, Tripp HJ, Steindler L, Smith DP, Giovannoni SJ. The presence of the glycolysis operon in SAR11 genomes is positively correlated with ocean productivity. Environ Microbiol. 2010;12:490–500.CAS 

    Google Scholar 
    Sun J, Todd JD, Thrash JC, Qian Y, Qian MC, Temperton B, et al. The abundant marine bacterium Pelagibacter simultaneously catabolizes dimethylsulfoniopropionate to the gases dimethyl sulfide and methanethiol. Nat Microbiol. 2016;1:16065.CAS 

    Google Scholar 
    Halsey KH, Giovannoni SJ, Graus M, Zhao Y, Landry Z, Thrash JC, et al. Biological cycling of volatile organic carbon by phytoplankton and bacterioplankton: VOC cycling by marine plankton. Limnol Oceanogr. 2017;62:2650–61.CAS 

    Google Scholar 
    Carlson CA, Giovannoni SJ, Hansell DA, Goldberg SJ, Parsons R, Vergin K. Interactions among dissolved organic carbon, microbial processes, and community structure in the mesopelagic zone of the northwestern Sargasso Sea. Limnol Oceanogr. 2004;49:1073–83.CAS 

    Google Scholar 
    Wagner S, Schubotz F, Kaiser K, Hallmann C, Waska H, Rossel PE, et al. Soothsaying DOM: a current perspective on the future of oceanic dissolved organic carbon. Front Mar Sci. 2020;7:341.
    Google Scholar 
    Quinn PK, Bates TS. The case against climate regulation via oceanic phytoplankton sulphur emissions. Nature. 2011;480:51–6.CAS 

    Google Scholar 
    Bolaños LM, Choi CJ, Worden AZ, Baetge N, Carlson CA, Giovannoni S. Seasonality of the microbial community composition in the North Atlantic. Front Mar Sci. 2021;8:624164.
    Google Scholar 
    Tucker SJ, Freel KC, Monaghan EA, Sullivan CES, Ramfelt O, Rii YM, et al. Spatial and temporal dynamics of SAR11 marine bacteria across a nearshore to offshore transect in the tropical Pacific Ocean. PeerJ. 2021;9:e12274.
    Google Scholar 
    Giovannoni SJ, Vergin KL. Seasonality in ocean microbial communities. Science. 2012;335:671–6.CAS 

    Google Scholar 
    Eren AM, Maignien L, Sul WJ, Murphy LG, Grim SL, Morrison HG, et al. Oligotyping: differentiating between closely related microbial taxa using 16S RRNA gene data. Methods Ecol Evol. 2013;4:1111–9.
    Google Scholar 
    Vergin K, Done B, Carlson C, Giovannoni S. Spatiotemporal distributions of rare bacterioplankton populations indicate adaptive strategies in the oligotrophic ocean. Aquat Microb Ecol. 2013;71:1–13.
    Google Scholar 
    Salter I, Galand PE, Fagervold SK, Lebaron P, Obernosterer I, Oliver MJ, et al. Seasonal dynamics of active SAR11 ecotypes in the oligotrophic Northwest Mediterranean Sea. ISME J. 2015;9:347–60.CAS 

    Google Scholar 
    Ortmann AC, Santos TTL. Spatial and temporal patterns in the Pelagibacteraceae across an estuarine gradient. FEMS Microbiol Ecol. 2016;92:fiw133.
    Google Scholar 
    Vergin KL, Beszteri B, Monier A, Cameron Thrash J, Temperton B, Treusch AH, et al. High-resolution SAR11 ecotype dynamics at the Bermuda Atlantic Time-series Study site by phylogenetic placement of pyrosequences. ISME J. 2013;7:1322–32.CAS 

    Google Scholar 
    Needham DM, Fichot EB, Wang E, Berdjeb L, Cram JA, Fichot CG, et al. Dynamics and interactions of highly resolved marine plankton via automated high-frequency sampling. ISME J. 2018;12:2417–32.CAS 

    Google Scholar 
    Benway HM, Lorenzoni L, White AE, Fiedler B, Levine NM, Nicholson DP, et al. Ocean time series observations of changing marine ecosystems: an era of integration, synthesis, and societal applications. Front Mar Sci. 2019;12:6–393.
    Google Scholar 
    Steinberg DK, Carlson CA, Bates NR, Johnson RJ, Michaels AF, Knap AH. Overview of the US JGOFS Bermuda Atlantic Time-series Study (BATS): a decade-scale look at ocean biology and biogeochemistry. Deep Sea Res Part II Top Stud Oceanogr. 2001;48:1405–47.CAS 

    Google Scholar 
    Southward AJ, Langmead O, Hardman-Mountford NJ, Aiken J, Boalch GT, Dando PR, et al. Long-term oceanographic and ecological research in the Western English Channel. In: Advances in marine biology. Elsevier. 2005;47:1–105.Gilbert JA, Field D, Swift P, Newbold L, Oliver A, Smyth T, et al. The seasonal structure of microbial communities in the Western English Channel. Environ Microbiol. 2009;11:3132–9.CAS 

    Google Scholar 
    Gilbert JA, Steele JA, Caporaso JG, Steinbrück L, Reeder J, Temperton B, et al. Defining seasonal marine microbial community dynamics. ISME J. 2012;6:298–308.CAS 

    Google Scholar 
    Caporaso JG, Paszkiewicz K, Field D, Knight R, Gilbert JA. The Western English Channel contains a persistent microbial seed bank. ISME J. 2012;6:1089–93.CAS 

    Google Scholar 
    Warwick-Dugdale J, Solonenko N, Moore K, Chittick L, Gregory AC, Allen MJ, et al. Long-read viral metagenomics captures abundant and microdiverse viral populations and their niche-defining genomic islands. PeerJ. 2019;7:e6800.
    Google Scholar 
    Vergin KL, Done B, Carlson CA, Giovannoni SJ. Spatiotemporal distributions of rare bacterioplankton populations indicate adaptive strategies in the oligotrophic ocean. Aquat Microb Ecol. 2013;71:1–3.
    Google Scholar 
    Choi CJ, Jimenez V, Needham DM, Poirier C, Bachy C, Alexander H, et al. Seasonal and geographical transitions in eukaryotic phytoplankton community structure in the Atlantic and Pacific Oceans. Front Microbiol. 2020;11:542372.
    Google Scholar 
    Bolaños LM, Karp-Boss L, Choi CJ, Worden AZ, Graff JR, Haëntjens N, et al. Small phytoplankton dominate western North Atlantic biomass. ISME J. 2020;14:1663–74.
    Google Scholar 
    Matsen FA, Kodner RB, Armbrust E. pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree. BMC Bioinform. 2010;11:1–6.
    Google Scholar 
    Treusch AH, Vergin KL, Finlay LA, Donatz MG, Burton RM, Carlson CA, et al. Seasonality and vertical structure of microbial communities in an ocean gyre. ISME J. 2009;3:1148–63.
    Google Scholar 
    Giovannoni SJ, Rappe MS, Vergin KL, Adair NL. 16S rRNA genes reveal stratified open ocean bacterioplankton populations related to the Green Non-Sulfur bacteria. Proc Natl Acad Sci. 1996;93:7979–84.CAS 

    Google Scholar 
    Morris RM, Vergin KL, Cho J-C, Rappé MS, Carlson CA, Giovannoni SJ. Temporal and spatial response of bacterioplankton lineages to annual convective overturn at the Bermuda Atlantic Time-series Study site. Limnol Oceanogr. 2005;50:1687–96.CAS 

    Google Scholar 
    Daims H, Brühl A, Amann R, Schleifer K-H, Wagner M. The domain-specific probe EUB338 is insufficient for the detection of all bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol. 1999;22:434–44.CAS 

    Google Scholar 
    Lane DJ. Nucleic acid techniques in bacterial systematics. In: Nucleic acid techniques in bacterial systematics. New York: Wiley; p. 115–75.Callahan BJ, McMurdie PJ, Holmes SP. Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J. 2017;11:2639–43.
    Google Scholar 
    McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One. 2013;8:e61217.CAS 

    Google Scholar 
    Eren AM, Borisy GG, Huse SM, Mark Welch JL. Oligotyping analysis of the human oral microbiome. Proc Natl Acad Sci. 2014;111:E2875–84.CAS 

    Google Scholar 
    Buchholz HH, Michelsen ML, Bolaños LM, Browne E, Allen MJ, Temperton B. Efficient dilution-to-extinction isolation of novel virus–host model systems for fastidious heterotrophic bacteria. ISME J. 2021;15:1585–98.CAS 

    Google Scholar 
    R Core Team. R: a language and environment for statistical computing. Vienna, Austria; https://www.R-project.org/Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. Package “vegan”.Wickham H. ggplot2: ggplot2. Wiley Interdiscip Rev Comput Stat. 2011;3:180–5.
    Google Scholar 
    Wang W, Yan J. Shape-restricted regression splines with R package splines2. J Data Sci. 2021;19:498–517.
    Google Scholar 
    Auladell A, Sánchez P, Sánchez O, Gasol JM, Ferrera I. Long-term seasonal and interannual variability of marine aerobic anoxygenic photoheterotrophic bacteria. ISME J. 2019;13:1975–87.CAS 

    Google Scholar 
    Ahdesmaki M, Fokianos K, Strimmer K, Ahdesmaki MM. Package ‘GeneCycle’ 2015.Roesch A, Schmidbauer H and Roesch MA. Package ‘WaveletComp.’ 2014.Lomas MW, Bates NR, Johnson RJ, Knap AH, Steinberg DK, Carlson CA. Two decades and counting: 24-years of sustained open ocean biogeochemical measurements in the Sargasso Sea. Deep Sea Res Part II Top Stud Oceanogr. 2013;93:16–32.CAS 

    Google Scholar 
    Lomas MW, Bates NR, Johnson RJ, Steinberg DK, Tanioka T. Adaptive carbon export response to warming in the Sargasso Sea. Nature Commun. 2022;13:1–0.
    Google Scholar 
    Sargeant SL, Murrell JC, Nightingale PD, Dixon JL. Basin-scale variability of microbial methanol uptake in the Atlantic Ocean. Biogeosciences. 2018;15:5155–67.CAS 

    Google Scholar 
    Smyth TJ, Allen I, Atkinson A, Bruun JT, Harmer RA, Pingree RD, et al. Ocean net heat flux influences seasonal to interannual patterns of plankton abundance. PLoS One. 2014;9:e98709.
    Google Scholar 
    Van de Peer Y. A quantitative map of nucleotide substitution rates in bacterial rRNA. Nucleic Acids Res. 1996;24:3381–91.
    Google Scholar 
    Baker GC, Smith JJ, Cowan DA. Review and re-analysis of domain-specific 16S primers. J Microbiol Methods. 2003;55:541–55.CAS 

    Google Scholar 
    Vasileiadis S, Puglisi E, Arena M, Cappa F, Cocconcelli PS, Trevisan M. Soil bacterial diversity screening using single 16S rRNA gene V regions coupled with multi-million read generating sequencing technologies. PLoS ONE. 2012;7:e42671.CAS 

    Google Scholar 
    Stingl U, Tripp HJ, Giovannoni SJ. Improvements of high-throughput culturing yielded novel SAR11 strains and other abundant marine bacteria from the Oregon coast and the Bermuda Atlantic Time-series study site. ISME J. 2007;1:361–71.CAS 

    Google Scholar 
    Delmont TO, Kiefl E, Kilinc O, Esen OC, Uysal I, Rappé MS, et al. Single-amino acid variants reveal evolutionary processes that shape the biogeography of a global SAR11 subclade. eLife. 2019;8:e46497.
    Google Scholar 
    Lévy M, Jahn O, Dutkiewicz S, Follows MJ, d’Ovidio F. The dynamical landscape of marine phytoplankton diversity. J R Soc Interface. 2015;12:20150481.
    Google Scholar 
    Hellweger FL, van Sebille E, Calfee BC, Chandler JW, Zinser ER, Swan BK, et al. The role of ocean currents in the temperature selection of plankton: insights from an individual-based model. PLoS ONE. 2016;11:e0167010.
    Google Scholar 
    Giovannoni SJ, Tripp HJ, Givan S, Podar M, Vergin KL, Baptista D, et al. Genome streamlining in a cosmopolitan oceanic bacterium. Science. 2005;309:1242–5.CAS 

    Google Scholar 
    Brown SN, Giovannoni S, Cho JC. Polyphasic taxonomy of marine bacteria from the SAR11 group Ia: Pelagibacter ubiquis (strain HTCC1062) & Pelagibacter bermudensis (strain HTCC7211). Oregon State University; 2012.Auladell A, Barberán A, Logares R, Garcés E, Gasol JM, Ferrera I. Seasonal niche differentiation among closely related marine bacteria. ISME J. 2022;16:178–89.CAS 

    Google Scholar 
    Tsementzi D, Wu J, Deutsch S, Nath S, Rodriguez-R LM, Burns AS, et al. SAR11 bacteria linked to ocean anoxia and nitrogen loss. Nature. 2016;536:179–83.CAS 

    Google Scholar 
    Ruiz-Perez CA, Bertagnolli AD, Tsementzi D, Woyke T, Stewart FJ, Konstantinidis KT. Description of Candidatus Mesopelagibacter carboxydoxydans and Candidatus Anoxipelagibacter denitrificans: nitrate-reducing SAR11 genera that dominate mesopelagic and anoxic marine zones. Syst Appl Microbiol. 2021;44:126185.CAS 

    Google Scholar 
    Yeh YC, Fuhrman JA. Contrasting diversity patterns of prokaryotes and protists over time and depth at the San-Pedro Ocean Time series. ISME Commun. 2022;13:1–12.
    Google Scholar 
    McCarthy M, Spillane S, Walsh S, Kendon M. The meteorology of the exceptional winter of 2015/2016 across the UK and Ireland. Weather. 2016;71:305–13.
    Google Scholar 
    Met Office. UK Climate Projections: Headline Findings. 2021. More

  • in

    Defensive functions and potential ecological conflicts of floral stickiness

    Gorb, E. V. & Gorb, S. N. Anti-adhesive effects of plant wax coverage on insect attachment. J. Exp. Bot. 68, 5323–5337 (2017).CAS 
    PubMed 

    Google Scholar 
    Agrawal, A. A. & Konno, K. Latex: A model for understanding mechanisms, ecology, and evolution of plant defense against herbivory. Annu. Rev. Ecol. Evol. Syst. 40, 311–331 (2009).
    Google Scholar 
    Langenheim, J. H. Plant resins. Am. Sci. 78, 16–24 (1990).
    Google Scholar 
    Ben-Mahmoud, S. et al. Acylsugar amount and fatty acid profile differentially suppress oviposition by western flower thrips, Frankliniella occidentalis, on tomato and interspecific hybrid flowers. PLoS ONE 13, 1–20 (2018).
    Google Scholar 
    LoPresti, E. F., Pearse, I. S. & Charles, G. K. The siren song of a sticky plant: Columbines provision mutualist arthropods by attracting and killing passerby insects. Ecology 96, 2862–2869 (2015).CAS 
    PubMed 

    Google Scholar 
    Weinhold, A. & Baldwin, I. T. Trichome-derived O-acyl sugars are a first meal for caterpillars that tags them for predation. Proc. Natl. Acad. Sci. 108, 7855–7859 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Krimmel, B. A. & Wheeler, A. G. Host-plant stickiness disrupts novel ant–mealybug association. Arthropod. Plant. Interact. 9, 187–195 (2015).
    Google Scholar 
    Simmons, A. T., Gurr, G. M., McGrath, D., Martin, P. M. & Nicol, H. I. Entrapment of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) on glandular trichomes of Lycopersicon species. Aust. J. Entomol. 43, 196–200 (2004).
    Google Scholar 
    Carter, C. D., Gianfagna, T. J. & Sacalis, J. N. Sesquiterpenes in glandular trichomes of a wild tomato species and toxicity to the colorado potato beetle. J. Agric. Food Chem. 37, 1425–1428 (1989).CAS 

    Google Scholar 
    Van Dam, N. M. & Hare, J. D. Biological activity of Datura wrightii glandular trichome exudate against Manduca sexta larvae. J. Chem. Ecol. 24, 1529–1549 (1998).
    Google Scholar 
    Kessler, A. & Heil, M. The multiple faces of indirect defences and their agents of natural selection. Funct. Ecol. 25, 348–357 (2011).
    Google Scholar 
    Karban, R., LoPresti, E., Pepi, A. & Grof-Tisza, P. Induction of the sticky plant defense syndrome in wild tobacco. Ecology 100, 1–9 (2019).
    Google Scholar 
    Krimmel, B. A. & Pearse, I. S. Sticky plant traps insects to enhance indirect defence. Ecol. Lett. 16, 219–224 (2013).CAS 
    PubMed 

    Google Scholar 
    Eisner, T. & Aneshansley, D. J. Adhesive strength of the insect-trapping glue of a plant (Befaria racemosa). Ann. Entomol. Soc. Am. 76, 295–298 (1983).
    Google Scholar 
    Spomer, G. G. Evidence of protocarnivorous capabilities in Geranium viscosissimum and Potentilla arguta and other sticky plants. Int. J. Plant Sci. 160, 98–101 (1999).
    Google Scholar 
    Darnowski, D. W., Carroll, D. M., Płachno, B., Kabanoff, E. & Cinnamon, E. Evidence of protocarnivory in triggerplants (Stylidium spp.; Stylidiaceae). Plant Biol. 8, 805–812 (2006).CAS 
    PubMed 

    Google Scholar 
    Givnish, T. J., Burkhardt, E. L., Happel, R. E. & Weintraub, J. D. Carnivory in the bromeliad Brocchinia reducta, with a cost/benefit model for the general restriction of carnivorous plants to sunny, moist nutrient-poor habitats. Am. Nat. 124, 479–497 (1984).
    Google Scholar 
    Jürgens, N. Psammophorous plants and other adaptations to desert ecosystems with high incidence of sandstorms. Feddes Repert. 107, 345–359 (1996).
    Google Scholar 
    Lopresti, E. F. & Karban, R. Chewing sandpaper: Grit, plant apparency, and plant defense in sand-entrapping plants. Ecology 97, 826–833 (2016).PubMed 

    Google Scholar 
    Krupnick, G. A. & Weis, A. E. The effect of floral herbivory on male and female reproductive success in Isomeris arborea. Ecology 80, 135–149 (1999).
    Google Scholar 
    McCall, A. C. Florivory affects pollinator visitation and female fitness in Nemophila menziesii. Oecologia 155, 729–737 (2008).ADS 
    PubMed 

    Google Scholar 
    Bandeili, B. & Müller, C. Folivory versus florivory-adaptiveness of flower feeding. Naturwissenschaften 97, 79–88 (2010).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Lai, D. et al. Lotus japonicus flowers are defended by a cyanogenic β-glucosidase with highly restricted expression to essential reproductive organs. Plant Mol. Biol. 89, 21–34 (2015).CAS 
    PubMed 

    Google Scholar 
    Kessler, A. & Halitschke, R. Testing the potential for conflicting selection on floral chemical traits by pollinators and herbivores: Predictions and case study. Funct. Ecol. 23, 901–912 (2009).
    Google Scholar 
    Kessler, D., Diezel, C., Clark, D. G., Colquhoun, T. A. & Baldwin, I. T. Petunia flowers solve the defence/apparency dilemma of pollinator attraction by deploying complex floral blends. Ecol. Lett. 16, 299–306 (2013).PubMed 

    Google Scholar 
    Li, J. et al. Defense of pyrethrum flowers: Repelling herbivores and recruiting carnivores by producing aphid alarm pheromone. New Phytol. 223, 1607–1620 (2019).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kennedy, G. G. Tomato, pests, parasitoids, and predators: tritrophic interactions involving the genus Lycopersicon. Annu. Rev. Entomol. 48, 51–72 (2003).CAS 
    PubMed 

    Google Scholar 
    McCarren, S., Coetzee, A. & Midgley, J. Corolla stickiness prevents nectar robbing in Erica. J. Plant Res. https://doi.org/10.1007/s10265-021-01299-z (2021).Article 
    PubMed 

    Google Scholar 
    Matulevich Peláez, J. A., Gil Archila, E. & Ospina Giraldo, L. F. Estudio fitoquímico de hojas, flores y frutos de Bejaria resinosa mutis ex linné filius (ericaceae) y evaluación de su actividad antiinflamatoria. Rev. Cuba. Plantas Med. 21, 332–345 (2016).
    Google Scholar 
    Kraemer, M. On the pollination of Bejaria resinosa Mutis ex Linne f. ( Ericaceae ), an ornithophilous Andean paramo shrub. Flora 196, 59–62 (2001).
    Google Scholar 
    Melampy, A. M. N. Flowering phenology, pollen flow and fruit production in the Andean Shrub Befaria resinosa. Oecologia 73, 293–300 (1987).ADS 
    CAS 
    PubMed 

    Google Scholar 
    LoPresti, E. F., Robinson, M. L., Krimmel, B. A. & Charles, G. K. The sticky fruit of manzanita: potential functions beyond epizoochory. Ecology 99, 2128–2130 (2018).PubMed 

    Google Scholar 
    Kessler, A. & Chautá, A. The ecological consequences of herbivore-induced plant responses on plant-pollinator interactions. Emerg. Topics Life Sci. 4, 33–43 (2020).
    Google Scholar 
    Lucas-Barbosa, D. Integrating studies on plant-pollinator and plant-herbivore interactions. Trends Plant Sci. 21, 125–133 (2016).CAS 
    PubMed 

    Google Scholar 
    Leckie, B. M. et al. Differential and synergistic functionality of acylsugars in suppressing oviposition by insect herbivores. PLoS ONE 11, 1–19 (2016).
    Google Scholar 
    Monteiro, R. F. & Macedo, M. V. First report on the diversity of insects trapped by a sticky exudate of the inflorescences of Vriesea bituminosa Wawra (Bromeliaceae: Tillandsioideae). Arthropod. Plant. Interact. 8, 519–523 (2014).
    Google Scholar 
    Chatzivasileiadis, E. A. & Sabelis, M. W. Toxicity of methyl ketones from tomato trichomes to Tetranychus urticae Koch. Exp. Appl. Acarol. 21, 473–484 (1997).CAS 

    Google Scholar 
    Avé, D. A., Gregory, P. & Tingey, W. M. Aphid repellent sesquiterpenes in glandular trichomes of Solanum berthaultii and S. tuberosum. Entomol. Exp. Appl. 44, 131–138 (1987).
    Google Scholar 
    LoPresti, E. Columbine pollination success not determined by a proteinaceous reward to hummingbird pollinators. J. Pollinat. Ecol. 20, 35–39 (2017).
    Google Scholar 
    Krimmel, B. A. & Pearse, I. S. Generalist and sticky plant specialist predators suppress herbivores on a sticky plant. Arthropod. Plant. Interact. 8, 403–410 (2014).
    Google Scholar 
    Adlassnig, W., Lendl, T., Peroutka, M. & Lang, I. Deadly glue- Adhesive traps of carnivorous plants. in Biological Adhesive Systems (eds. von Byren, J. & Grunwald, I.) 15–28 (2010).Ellison, A. M. & Gotelli, N. J. Evolutionary ecology of carnivorous plants. Trends Ecol. Evol. 16, 623–629 (2001).
    Google Scholar 
    Maloof, J. E. & Inouye, D. W. Are nectar robbers cheaters or mutualists?. Ecology 81, 2651–2661 (2000).
    Google Scholar 
    Asai, T., Hirayama, Y. & Fujimoto, Y. Epi-α-bisabolol 6-deoxy-β-d-gulopyranoside from the glandular trichome exudate of Brillantaisia owariensis. Phytochem. Lett. 5, 376–378 (2012).CAS 

    Google Scholar 
    Asai, T., Hara, N. & Fujimoto, Y. Fatty acid derivatives and dammarane triterpenes from the glandular trichome exudates of Ibicella lutea and Proboscidea louisiana. Phytochemistry 71, 877–894 (2010).CAS 
    PubMed 

    Google Scholar 
    Ohkawa, A., Sakai, T., Ohyama, K. & Fujimoto, Y. Malonylated glycerolipids from the glandular trichome exudate of Ceratotheca triloba. Chem. Biodivers. 9, 1611–1617 (2012).CAS 
    PubMed 

    Google Scholar 
    Omosa, L. K. et al. Antimicrobial flavonoids and diterpenoids from Dodonaea angustifolia. S. Afr. J. Bot. 91, 58–62 (2014).CAS 

    Google Scholar 
    Kessler, A. The information landscape of plant constitutive and induced secondary metabolite production. Curr. Opin. Insect Sci. 8, 47–53 (2015).PubMed 

    Google Scholar 
    Knudsen, J. T., Tollsten, L., Groth, I., Bergström, G. & Raguso, R. A. Trends in floral scent chemistry in pollination syndromes: Floral scent composition in hummingbird-pollinated taxa. Bot. J. Linn. Soc. 146, 191–199 (2004).
    Google Scholar 
    Pearse, I. S., Gee, W. S. & Beck, J. J. Headspace volatiles from 52 oak species advertise induction, species identity, and evolution, but not defense. J. Chem. Ecol. 39, 90–100 (2013).CAS 
    PubMed 

    Google Scholar 
    El-Sayed, A. M., Byers, J. A. & Suckling, D. M. Pollinator-prey conflicts in carnivorous plants: When flower and trap properties mean life or death. Sci. Rep. 6, 1–11 (2016).
    Google Scholar 
    Greenaway, W., May, J. & Whatley, F. R. Analysis of phenolics of bud exudate of Populus tristis by GC/MS. Zeitschrift fur Naturforsch.. Sect C J. Biosci. 47, 512–515 (1992).
    Google Scholar 
    Urzua, A. & Cuadra, P. Acylated flavonoid aglycones from Gnaphalium robustum. Phytochem. Divers. Redundancy Ecol. Interact. 29, 1342–1343 (1990).CAS 

    Google Scholar 
    Drewes, S. E., Mudau, K. E., Van Vuuren, S. F. & Viljoen, A. M. Antimicrobial monomeric and dimeric diterpenes from the leaves of Helichrysum tenax var tenax. Phytochemistry 67, 716–722 (2006).CAS 
    PubMed 

    Google Scholar 
    Midiwo, J. O. et al. Bioactive compounds from some Kenyan ethnomedicinal plants: Myrsinaceae, Polygonaceae and Psiadia punctulata. Phytochem. Rev. 1, 311–323 (2002).CAS 

    Google Scholar 
    Jiménez-Pomárico, A. et al. Chemical and morpho-functional aspects of the interaction between a Neotropical resin bug and a sticky plant. Rev. Biol. Trop. 67, 454–465 (2019).
    Google Scholar 
    Linhart, Y. B., Thompson, J. D., Url, S. & John, D. Terpene-based selective herbivory by Helix aspersa (Mollusca) on Thymus vulgaris (Labiatae). Oecologia 102, 126–132 (2012).
    Google Scholar 
    Kessler, A., Halitschke, R. & Poveda, K. Herbivory-mediated pollinator limitation: Negative impacts of induced volatiles on plant-pollinator interactions. Ecology 92, 1769–1780 (2011).PubMed 

    Google Scholar 
    Sletvold, N., Moritz, K. K. & Ågren, J. Additive effects of pollinators and herbivores result in both conflicting and reinforcing selection on floral traits. Ecology 96, 214–221 (2015).PubMed 

    Google Scholar 
    Ramos, S. E. & Schiestl, F. P. Rapid plant evolution driven by the interaction of pollination and herbivory. Science (80-). 364, 193–196 (2019).ADS 
    CAS 

    Google Scholar 
    Rojas-Nossa, S. V. Estrategias de extracción de néctar por pinchaflores (Aves: Diglossa y Diglossopis) y sus efectos sobre la polinización de plantas de los altos Andes. Ornitol. Colomb. 5, 21–39 (2007).
    Google Scholar 
    R Team Core. R: A language and environment for statistical computing. R Foundation for Statistical Computing. (2021).Liaw, A. & Wiener, M. Classification and regression by randomForest. R News 2, 18–22 (2002).
    Google Scholar 
    Diaz-Uriarte, R. Package ‘ varSelRF ’. Compr. R Arch. Netw. 1–23 (2015). More

  • in

    Quantifying thermal cues that initiate mass emigrations in juvenile white sharks

    Chen, I. C., Hill, J. K., Ohlemüller, R., Roy, D. B. & Thomas, C. D. Rapid range shifts of species associated with high levels of climate warming. Science 333(6045), 1024–1026. https://doi.org/10.1126/SCIENCE.1206432 (2011).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Newton, I. Migration within the annual cycle: Species, sex and age differences. J. Ornithol. 152, 169–185. https://doi.org/10.1007/S10336-011-0689-Y/TABLES/1 (2011).Article 

    Google Scholar 
    Dodson, S., Abrahms, B., Bograd, S. J., Fiechter, J. & Hazen, E. L. Disentangling the biotic and abiotic drivers of emergent migratory behavior using individual-based models. Ecol. Model. 432, 109225. https://doi.org/10.1016/J.ECOLMODEL.2020.109225 (2020).Article 

    Google Scholar 
    Lehikoinen, A. et al. Sex-specific timing of autumn migration in birds: the role of sexual size dimorphism, migration distance and differences in breeding investment. Ornis Fennica 94, 53–65 (2017).
    Google Scholar 
    Stewart, B. S. Ontogeny of differential migration and sexual segregation in northern elephant seals. J. Mammol. 78(4), 1101–1116 (1997).Somveille, M., Rodrigues, A. S. L. & Manica, A. Why do birds migrate? A macroecological perspective. Glob. Ecol. Biogeogr. 24(6), 664–674. https://doi.org/10.1111/geb.12298 (2015).Article 

    Google Scholar 
    Corkeron, P. J. & Connor, R. C. Why do baleen whales migrate?. Mar. Mamm. Sci. 15(4), 1228–1245. https://doi.org/10.1111/J.1748-7692.1999.TB00887.X (1999).Article 

    Google Scholar 
    Mourier, J., Mills, S. C. & Planes, S. Population structure, spatial distribution and life-history traits of blacktip reef sharks Carcharhinus melanopterus. J. Fish Biol. 82(3), 979–993. https://doi.org/10.1111/JFB.12039 (2013).Article 
    CAS 
    PubMed 

    Google Scholar 
    Avgar, T., Mosser, A., Brown, G. S. & Fryxell, J. M. Environmental and individual drivers of animal movement patterns across a wide geographical gradient. J. Anim. Ecol. 82, 96–106. https://doi.org/10.1111/j.1365-2656.2012.02035.x (2013).Article 
    PubMed 

    Google Scholar 
    Crawshaw, L. I. Physiological and behavioral reactions of fishes to temperature change. J. Fish. Res. Board Can. 34(5), 730–734. https://doi.org/10.1139/f77-113 (1977).Article 

    Google Scholar 
    Heithaus, M., Dill, L., Marshall, G. J. & Buhleier, B. Habitat use and foraging behavior of tiger sharks (Galeocerdo cuvier) in a seagrass ecosystem. Mar. Biol. 140, 337–348. https://doi.org/10.1007/s00227-001-0711-7 (2002).Article 

    Google Scholar 
    Magnuson, J. J., Crowder, L. B. & Medvick, P. A. Temperature as an ecological resource. Integr. Comp. Biol. 19(1), 331–343. https://doi.org/10.1093/icb/19.1.331 (1979).Article 

    Google Scholar 
    Matern, S. A., Cech, J. J. & Hopkins, T. E. Diel movements of bat rays, Myliobatis californica, in Tomales Bay, California: Evidence for behavioral thermoregulation?. Environ. Biol. Fishes 58(2), 173–182. https://doi.org/10.1023/A:1007625212099 (2000).Article 

    Google Scholar 
    Speed, C. W., Meekan, M. G., Field, I. C., McMahon, C. R. & Bradshaw, C. J. A. Heat-seeking sharks: Support for behavioural thermoregulation in reef sharks. Mar. Ecol. Prog. Ser. 463, 231–244. https://doi.org/10.3354/meps09864 (2012).Article 
    ADS 

    Google Scholar 
    Dewar, H., Domeier, M. & Nasby-Lucas, N. Insights into young of the year white shark, Carcharodon carcharias, behavior in the Southern California Bight. Environ. Biol. Fishes https://doi.org/10.1023/B:EBFI.0000029343.54027.6a.pdf (2004).Article 

    Google Scholar 
    Hertz, P. E., Huey, R. & Stevenson, R. D. Evaluating temperature regulation by field-active ectotherms. Am. Nat. 142, 796–818 (1993).Article 
    CAS 
    PubMed 

    Google Scholar 
    Heupel, M. R., Simpfendorfer, C. A. & Hueter, R. E. Estimation of shark home ranges using passive monitoring techniques. Environ. Biol. Fishes 71(2), 135–142. https://doi.org/10.1023/b:ebfi.0000045710.18997.f7 (2004).Article 

    Google Scholar 
    Topping, D. T., Lowe, C. G. & Caselle, J. E. Site fidelity and seasonal movement patterns of adult California sheephead Semicossyphus pulcher (Labridae): An acoustic monitoring study. Mar. Ecol. Progr. Ser. 326, 257–267 (2006).Weng, K. C. et al. Movements, behavior and habitat preferences of juvenile white sharks Carcharodon carcharias in the eastern Pacific. Mar. Ecol. Prog. Ser. 338, 211–224. https://doi.org/10.3354/meps338211 (2007).Article 
    ADS 

    Google Scholar 
    Lyons, K. et al. The degree and result of gillnet fishery interactions with juvenile white sharks in southern California assessed by fishery-independent and -dependent methods. Fish. Res. 147, 370–380. https://doi.org/10.1016/J.FISHRES.2013.07.009 (2013).Article 
    ADS 

    Google Scholar 
    Papastamatiou, Y. P. et al. Drivers of daily routines in an ectothermic marine predator: Hunt warm, rest warmer?. PLoS ONE. https://doi.org/10.1371/journal.pone.0127807 (2015).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Adolph, S. C. Influence of behavioral thermoregulation on microhabitat use by two sceloporus lizards. Ecology 71(1), 315–327. https://doi.org/10.2307/1940271 (1990).Article 

    Google Scholar 
    Heithaus, M. R. The biology of tiger sharks, Galeocerdo cuvier, in Shark Bay, Western Australia: sex ratio, size distribution, diet, and seasonal changes in catch rates. Environ. Biol. Fishes 61, 25–36 (2001).Article 

    Google Scholar 
    Vaudo, J. J. & Lowe, C. G. Movement patterns of the round stingray Urobatis halleri(Cooper) near a thermal outfall. J. Fish Biol. 68(6), 1756–1766. https://doi.org/10.1111/j.0022-1112.2006.01054.x (2006).Article 

    Google Scholar 
    Vaudo, J. J. & Heithaus, M. R. Microhabitat selection by marine mesoconsumers in a thermally heterogeneous habitat: Behavioral thermoregulation or avoiding predation risk?. PLoS ONE. 8(4), e61907. https://doi.org/10.1371/journal.pone.0061907 (2013).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Weng, K. C. et al. Migration and habitat of white sharks (Carcharodon carcharias) in the eastern Pacific Ocean. Mar. Biol. 152(4), 877–894. https://doi.org/10.1007/s00227-007-0739-4 (2007).Article 

    Google Scholar 
    White, C. F. et al. Quantifying habitat selection and variability in habitat suitability for juvenile white sharks. PLoS ONE 14(5), e0214642. https://doi.org/10.1371/journal.pone.0214642 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Curtis, T. H. et al. First insights into the movements of young-of-the-year white sharks (Carcharodon carcharias) in the western North Atlantic Ocean. Sci. Rep. 8(1), 1–8. https://doi.org/10.1038/s41598-018-29180-5 (2018).Article 
    ADS 
    CAS 

    Google Scholar 
    Bruce, B. D., Harasti, D., Lee, K., Gallen, C. & Bradford, R. Broad-scale movements of juvenile white sharks Carcharodon carcharias in eastern Australia from acoustic and satellite telemetry. Mar. Ecol. Prog. Ser. 619, 1–15. https://doi.org/10.3354/MEPS12969 (2019).Article 
    ADS 

    Google Scholar 
    Carey, F. G. et al. Temperature and activities of a white shark Carcharodon carcharias. Copeia 2, 254–260. https://doi.org/10.2307/1444603 (1982).Article 

    Google Scholar 
    Klimley, A. P., Beavers, S. C., Curtis, T. H. & Jorgensen, S. J. Movements and swimming behavior of three species of sharks in La Jolla Canyon, California. Environ. Biol. Fish. 63, 117–135. https://doi.org/10.1023/A:1014200301213.pdf (2002).Article 

    Google Scholar 
    Towner, A. V., Underhill, L. G., Jewell, O. J. D. & Smale, M. J. Environmental Influences on the abundance and sexual composition of white sharks Carcharodon carcharias in Gansbaai, South Africa. PLoS ONE. 8(8), e71197. https://doi.org/10.1371/journal.pone.0071197 (2013).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Anderson, J. M. et al. High-resolution acoustic telemetry reveals swim speeds and inferred field metabolic rates in juvenile white sharks (Carcharodon carcharias). PLoS ONE 17(6), e0268914. https://doi.org/10.1371/JOURNAL.PONE.0268914 (2022).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Anderson, J. M. et al. Interannual nearshore habitat use of young of the year white sharks off Southern California. Front. Mar. Sci. 8, 238. https://doi.org/10.3389/fmars.2021.645142 (2021).Article 

    Google Scholar 
    Domeier, M. L. & Nasby-Lucas, N. Two-year migration of adult female white sharks (Carcharodon carcharias) reveals widely separated nursery areas and conservation concerns. Anim. Biotelemet. 1(1), 1–10. https://doi.org/10.1186/2050-3385-1-2/FIGURES/3 (2013).Article 

    Google Scholar 
    Oñate-González, E. C. et al. Importance of Bahia Sebastian Vizcaino as a nursery area for white sharks (Carcharodon carcharias) in the Northeastern Pacific: A fishery dependent analysis. Fish. Res. 188, 125–137. https://doi.org/10.1016/J.FISHRES.2016.12.014 (2017).Article 

    Google Scholar 
    Lowe, C. G. et al. Historic fishery interactions with white sharks in the Southern California Bight. Glob. Perspect. Biol. Life Hist. White Shark 14, 169–190 (2012).
    Google Scholar 
    Anderson, J. M. et al. Non-random Co-occurrence of Juvenile White Sharks (Carcharodon carcharias) at Seasonal Aggregation Sites in Southern California. Front. Mar. Sci. 8, 1–14. https://doi.org/10.3389/fmars.2021.688505 (2021).Article 
    ADS 
    CAS 

    Google Scholar 
    Benson, J. F. et al. Juvenile survival, competing risks, and spatial variation in mortality risk of a marine apex predator. J. Appl. Ecol. 55, 2888–2897. https://doi.org/10.1111/1365-2664.13158 (2018).Article 

    Google Scholar 
    RStudio Team. RStudio: Integrated Development for R. (RStudio, PBC, 2020) http://www.rstudio.com/.Derrick, T., & Thomas, J. Time Series Analysis: The Cross-Correlation Function. Innovative Analyses of Human Movement, Chapter 7. https://lib.dr.iastate.edu/kin_pubs/46 (2004).Killick, R., Fearnhead, P. & Eckley, I. A. Optimal detection of changepoints with a linear computational cost. J. Am. Stat. Assoc. 107, 1590–1598. https://doi.org/10.1080/01621459.2012.737745 (2012).Article 
    MathSciNet 
    CAS 
    MATH 

    Google Scholar 
    Bakun, A. Coastal Upwelling Indices, West Coast of North America. US Department of Commerce. NOAA Technical Report, NMFS SSRF-671 (1973).Di Lorenzo, E. Seasonal dynamics of the surface circulation in the Southern California Current System. Deep-Sea Res. Part II 50(14–16), 2371–2388. https://doi.org/10.1016/S0967-0645(03)00125-5 (2003).Article 
    ADS 

    Google Scholar 
    Lynn, R. J. & Simpson, J. J. The California Current System: The seasonal variability of its physical characteristics. J. Geophys. Res. 92(C12), 12947. https://doi.org/10.1029/jc092ic12p12947 (1987).Article 
    ADS 

    Google Scholar 
    Sinnett, G. & Feddersen, F. The surf zone heat budget: The effect of wave heating. Geophys. Res. Lett. 41(20), 7217–7226. https://doi.org/10.1002/2014GL061398 (2014).Article 
    ADS 

    Google Scholar 
    Wei, X., Li, K.-Y., Kilpatrick, T., Wang, M. & Xie, S.-P. Large-scale conditions for the record-setting Southern California marine heatwave of August 2018. Geophys. Res. Lett. 48(7), e2020GL091803 (2021).Article 
    ADS 

    Google Scholar 
    Freedman, R. M., Brown, J. A., Caldow, C. & Caselle, J. E. Marine protected areas do not prevent marine heatwave-induced fish community structure changes in a temperate transition zone. Sci. Rep. 10(1), 1–8. https://doi.org/10.1038/s41598-020-77885-3 (2020).Article 
    CAS 

    Google Scholar 
    Heupel, M. R., Simpfendorfer, C. A. & Hueter, R. E. Running before the storm: blacktip sharks respond to falling barometric pressure associated with Tropical Storm Gabrielle. J. Fish Biol. 63(5), 1357–1363. https://doi.org/10.1046/J.1095-8649.2003.00250.X (2003).Article 

    Google Scholar 
    Guttridge, T. L. et al. Deep danger: Intra-specific predation risk influences habitat use and aggregation formation of juvenile lemon sharks Negaprion brevirostris. Mar. Ecol. Progr. Ser. 445, 279–291 (2012).Article 
    ADS 

    Google Scholar 
    Grainger, R. et al. Diet composition and nutritional niche breadth variability in juvenile white sharks (Carcharodon carcharias). Front. Mar. Sci. 7, 422 (2020).Article 

    Google Scholar 
    Hussey, N. E., Christiansen, H. M. & Dudley, S. F. J. Size-based analysis of diet and trophic position of the white shark, carcharodon carcharias, in South African waters. Glob. Perspect. Biol. Life Hist. White Shark 3, 27–49. https://doi.org/10.1201/b11532-5 (2012).Article 

    Google Scholar 
    Kim, S. L., Tinker, M. T., Estes, J. A. & Koch, P. L. Ontogenetic and among-individual variation in foraging strategies of northeast Pacific white sharks based on stable isotope analysis. PLoS ONE 7(9), e45068. https://doi.org/10.1371/JOURNAL.PONE.0045068 (2012).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Tinker, M. T. et al. Dramatic increase in sea otter mortality from white sharks in California. Mar. Mamm. Sci. 32(1), 309–326. https://doi.org/10.1111/mms.12261 (2015).Article 

    Google Scholar  More

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    Global crop yields can be lifted by timely adaptation of growing periods to climate change

    Rule-based mean sowing and maturity datesLocation- and climate-specific mean crop calendars are computed by combining two rule-based approaches published by19 and22 to simulate sowing and physiological maturity dates of grain crops, respectively. The assumption is that farmers select growing seasons based on the mean climatic characteristics of their specific location and on the physiological limitations (base and optimum temperatures for reproductive growth; sensitivity to terminal water stress) of the respective crop species. Accordingly, they select sowing dates and cultivars with phenologies that, on average, meet these adapted maturity dates.The climate is classified into (i) seasonality types, based on the coefficient of variation of monthly mean temperature and precipitation and (ii) temperature levels, based on the temperature of the warmest month as compared to the base and the optimum temperatures for the crop reproductive growth. Optimal temperatures for sowing, optimal temperature ranges for grain filling, as well as indicators of soil moisture conditions (based on precipitation/potential-evapotranspiration ratio (P/PET)), are defined as global parameters for each crop (Supplementary Table 1) and used as thresholds to identify the best timing for sowing and for the start or end of the crop grain-filling phase. To cope with fluctuations of daily values around these thresholds, mean daily temperature, precipitation and potential evapotranspiration are derived by linear interpolation between monthly values.We distinguish between spring and winter crop types. Maize, rice, sorghum, and soybean are simulated as spring crops only, for wheat we simulate both types. For spring crops, farmers sow the crops at the onset of the wet season (first day of the wettest 120 consecutive days), in case of prevailing precipitation seasonality, or on the day of the year when temperatures increase above crop-specific temperature threshold19 (Supplementary Table 1), in case of temperature-driven seasonality.For wheat, we distinguish three types: winter wheat with vernalization is chosen if monthly temperatures fall below 0 °C, but winter is neither too harsh (temperature of the coldest month is higher than −10 °C), nor too long (temperatures fall below the sowing temperature threshold (12 °C) after 15th September (North hemisphere) or 31st March (South hemisphere)19). Winter wheat without vernalization is grown if winters are mild (the temperature of the coldest month is higher than 0 °C) without dormancy. In this case, wheat is sown 75 days before the coldest month of the year. This rule was arbitrarily chosen based on observed wheat sowing dates in mild winter regions. If the conditions for growing any of the winter-wheat types are not met (winter too harsh and too long), then spring wheat (without vernalization) is chosen. Note that the computed sowing dates do not differ between rainfed and irrigated for any of the crops.The mean maturity date is chosen so that the crop grain-filling phase, the most critical for yield formation, occurs under the least stressful conditions possible in that location and climate as follows. Under precipitation seasonality, grain filling starts towards the end of the rainy season, when a P/PET threshold is crossed. Under temperature seasonality, (a) grain filling of spring crops starts in the warmest month of the year (if summer temperatures are optimal), or right after temperatures return within an optimal range; (b) grain filling of winter crops ends in the warmest month of the year (if summer temperatures are optimal), or right before temperatures exceed the optimal range; (c) eventually, maturity is advanced to escape terminal water stress. Note that the grain-filling phase has a static duration of 60 days for maize and 40 days for all the other crops. This assumption is based on empirical relationships between the total growth period and the post-flowering reproductive phase, showing that the partition between the vegetative and reproductive phase of grain crops follows a saturation curve that levels off after 90–100 days of total growth duration54. Different crops are assumed to have only one crop cycle (sowing-to-maturity) per year, therefore neither multi-cropping systems nor crop rotations are accounted for in the decision-making rules. A detailed description of the rules and parameterization can be found in refs. 19, 22.Simulated crop calendars reflect current farmers’ managementSimulated historical crop calendars, driven by the bias-corrected climate dataset WFDEI23, largely agree with observations11,12,13. We compare results both at the country and grid-cell level because, although the observed crop calendars used here are gridded datasets, their underlying sources are often reported per country. The country-level comparison highlights that the agreement is good for most countries, importantly, including those with large cropland area. The area-weighted Mean Absolute Error (MAE) is close or well below 30 days for all considered crops (Fig. 4). The simulated crop calendars compare well with the observed data also at the grid-cell level. Large areas, including major agricultural regions of importance for global yields, show deviations within ±15 days for both sowing and maturity dates (Supplementary Table 2 and Supplementary Figs. 21–24). However, evaluating the accuracy below 30 days is limited by the time resolution of the observations, which is either (i) monthly11 and converted by us into daily values, by taking the mid-day of the reported month, or (ii) daily12,13, but resulting from averages over large time windows (often  > 1 month). Overall, the accuracy of the model is in line with the original evaluations of this rule-base method19,22, as well as with other studies simulating average growing periods across large regions18,20.Fig. 4: Evaluation of simulated crop calendars.Country-level comparison of simulated and observed sowing (A) and maturity (B) dates (day of the year) for five crops. Each circle refers to a country and a crop, the size of the circle is scaled according to the cropland area per country. The area-weighted Mean Absolute Error (MAE, days) is reported for each crop. Crop-calendar simulations are based on WFDEI reanalysis climate forcing23 for the period 1979–2012. The observed crop calendar includes different sources11,12,13.Full size imageSimulation of daily crop phenology and yields with the LPJmL crop modelWe perform a modeling experiment across the global land grid at 0.5° × 0.5° resolution. We used the LPJmL5 crop model24,25 to simulate daily growth and phenological development of five crops, driven by climate projections from four General Circulation Models (GCMs) GFDL-ESM2M, HadGEM2-ES, IPSL-CM5A-LR and MIROC5 under the Representative Concentration Pathways 6.0 (RCP6.0) as provided in bias-adjusted form from the CMIP5 archive by the ISIMIP2b project42. Irrigated and rainfed production systems are simulated separately on their current harvested areas11, which is also used to compute total crop yields at grid-cell and global scale, as the product of yield by crop-specific area. A first 5000-year spin-up simulation is used to initialize all model pools (e.g., soil carbon and nitrogen content). A second spin-up simulation of 390 years is used to introduced effects of historical human-driven land-use change on these pools. A change in cropping area for the future scenarios is not considered in this study.Phenological development is simulated based on the thermal-time model, including the effect of vernalization. All crops are assumed to be insensitive to photoperiod, due to a lack of parameters for multiple-crops and global-scale simulations. Previous global studies15,18 that have focused on maize and wheat only, have found lower performances in the growing-period simulations when using a photo-thermal model, compared to a temperature-only driven approach and thus recommend caution when using the photoperiodic response. State-of-the-art global crop models13,16 also typically do not consider sensitivity to photoperiod or assume that the photoperiodic response of the cultivars chosen in each location are perfectly tuned to the given conditions.Sowing dates are prescribed based on the external rule-based algorithm. Crop cultivars are parametrized based on the phenological units required to reach the corresponding maturity dates (TUreq, °C days). In line with15, TUreq are derived consistently with the phenological module of the crop model LPJmL for each grid cell, crop, and rule-based computed growing period from the respective climate input. They are calculated as the sum of daily mean air temperature increments above a crop-specific base temperature (TU) (Supplementary Table 1) between rule-based sowing and maturity. In addition, winter-wheat cultivars require effective vernalization days (VUreq), that range between 0 (mild winters) and 70 (cold winters), depending on the temperature of the 5 coldest months (Eq. (1))15,18.$${{{{{mathrm{V}}}}}}{{{{{{mathrm{U}}}}}}}_{{{{{{{mathrm{req}}}}}}}}=frac{70}{5}times left(1-frac{{T}_{m}-3}{10-3}right)$$
    (1)
    where Tm is the mean temperature of the month.From the day of sowing, effective TU for phenological development are accumulated daily, as the difference between the mean air temperature on that day and the crop-specific base temperature for phenological development (Eq. (2)). The vernalization effectiveness is computed daily by a scaling factor (0–1), which is then multiplied to the TU (Eq. (2)). For crops that are insensitive to vernalization, VUd is set equal one.$${{{{{mathrm{T}}}}}}{{{{{{mathrm{U}}}}}}}_{{{{{{{mathrm{req}}}}}}}}=mathop{sum }_{d=1}^{{ndays}}left({max }left(0,{T}_{d}-{T}_{{base}}right)times mathop{sum }_{0}^{d}{{{{{mathrm{V}}}}}}{{{{{{mathrm{U}}}}}}}_{d}right)$$
    (2)
    where the scaling factor VUd is computed by a three-stage linear response function with a range of optimal temperatures (Eq. 3). Temperature for effective vernalization range between −4 °C and +17 °C, with an optimum range between 3 °C and 10 °C.$${{{{{{{mathrm{VU}}}}}}}}_{d}=left{begin{array}{cc}left({T}_{d}-left(-4right)right)/left(3-10right) & {{{{{{mathrm{if}}}}}}}-4 , < ,{T}_{d} , < , 3\ 1 & {{{{{{mathrm{if}}}}}}};3,le ,{T}_{d},le, 10\ left(17-{T}_{d}right)/left(17-10right) & {{{{{{mathrm{if}}}}}}};10 , < ,{T}_{d} , < , 17\ 0 & {{{{{{mathrm{otherwise}}}}}}}end{array}right}$$ (3) In this study, we have removed the effect of vernalization on slowing down TU accumulation until 10% of the total vernalization requirements is reached. In this way, the crop can accumulate both vernalization units and heat units in fall, so that there is some leaf growth before winter (in LPJmL, the LAI curve depends on accumulated heat units).The LPJmL model simulates phenology as one single phase from emergence to maturity. Although the flowering stage is not simulated as an explicit break point, the fraction of above-ground biomass that is allocated to the storage organs (fHI) depends on the phenological progress (fTUreq, fraction of TUreq that have been fulfilled), with the bulk of the storage organs start filling up after 40% of TUreq have been reached (Eq. (4)). In line with this, the LAI curve reaches a plateau when 45% (wheat) or 50% (other crops) of the TUreq are fulfilled, which could be considered a proxy of the flowering stage.$${{{{{{mathrm{fHI}}}}}}}=100times frac{{{{{{{{mathrm{fTU}}}}}}}}_{{{{{{{mathrm{req}}}}}}}}}{100times {{{{{{{mathrm{fTU}}}}}}}}_{{{{{{{mathrm{req}}}}}}}}+{{exp }}^{11.1-10.0times {{{{{{{mathrm{fTU}}}}}}}}_{{{{{{{mathrm{req}}}}}}}}}}$$ (4) Crop biomass growth is simulated by daily carbon accumulation and allocation to different plant organs (roots, leaves, storage organs, mobile reserves, and stem). The fraction of carbon allocated to each pool is a function of the fraction of completed phenological progress. Water stress increases allocation to the roots and reduces allocation to the leaves. The daily Net Primary Production (NPP) is the result of the Gross Primary Production (daily gross photosynthesis) reduced by the respiration costs. Gross photosynthesis is simulated as a function of absorbed photosynthetically active radiation, CO2 atmospheric mixing ratio, air temperature, day length, and canopy conductance. Photosynthesis rate is given by the minimum between light-limited and Rubisco-limited photosynthesis rates, with distinguished pathways for C3 and C4 crops. Respiration is tissue-specific and it is also driven by temperature. If accumulated NPP is insufficient to satisfy all organ demands, allocation follows a hierarchical order from roots, to leaves, to storage organs, and consequently penalizing the harvest index. Crops are subject to yield failure due to frost events (daily minimum temperature More

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    Minimal climate change impacts on the geographic distribution of Nepeta glomerulosa, medicinal species endemic to southwestern and central Asia

    Mahmoodi, S. et al. The current and future potential geographical distribution of Nepeta crispa Willd., an endemic, rare and threatened aromatic plant of Iran: Implications for ecological conservation and restoration. Ecol. Indic. 137, 108752 (2022).
    Google Scholar 
    Behroozian, M., Ejtehadi, H., Peterson, A. T., Memariani, F. & Mesdaghi, M. Climate change influences on the potential distribution of Dianthus polylepis Bien. ex Boiss.(Caryophyllaceae), an endemic species in the Irano-Turanian region. PLoS ONE 15, e0237527 (2020).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Khanal, S. et al. Potential impact of climate change on the distribution and conservation status of Pterocarpus marsupium, a Near Threatened South Asian medicinal tree species. Ecol. Inform. 70, 101722 (2022).
    Google Scholar 
    Dyderski, M. K., Paź, S., Frelich, L. E. & Jagodziński, A. M. How much does climate change threaten European forest tree species distributions?. Glob. Change Biol. 24, 1150–1163 (2018).ADS 

    Google Scholar 
    Sanjerehei, M. M. & Rundel, P. W. The impact of climate change on habitat suitability for Artemisia sieberi and Artemisia aucheri (Asteraceae)—A modeling approach. Pol. J. Ecol. 65, 97–109 (2017).
    Google Scholar 
    Erfanian, M. B., Sagharyan, M., Memariani, F. & Ejtehadi, H. Predicting range shifts of three endangered endemic plants of the Khorassan-Kopet Dagh floristic province under global change. Sci. Rep. 11, 1–13 (2021).
    Google Scholar 
    Zhang, J. M. et al. Effects of climate change on the distribution of wild Akebia trifoliata. Ecol. Evol. 12, e8714 (2022).PubMed 
    PubMed Central 

    Google Scholar 
    Li, J., Fan, G. & He, Y. Predicting the current and future distribution of three Coptis herbs in China under climate change conditions, using the MaxEnt model and chemical analysis. Sci. Total Environ. 698, 134141 (2020).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Yang, X.-Q., Kushwaha, S., Saran, S., Xu, J. & Roy, P. Maxent modeling for predicting the potential distribution of medicinal plant, Justicia adhatoda L. in Lesser Himalayan foothills. Ecol. Eng. 51, 83–87 (2013).CAS 

    Google Scholar 
    Greiser, C., Hylander, K., Meineri, E., Luoto, M. & Ehrlén, J. Climate limitation at the cold edge: Contrasting perspectives from species distribution modelling and a transplant experiment. Ecography 43, 637–647 (2020).
    Google Scholar 
    Guisan, A. & Thuiller, W. Predicting species distribution: Offering more than simple habitat models. Ecol. Lett. 8, 993–1009 (2005).PubMed 

    Google Scholar 
    Thuiller, W. et al. Predicting global change impacts on plant species’ distributions: Future challenges. Plant Ecol. Evol. Syst. 9, 137–152 (2008).
    Google Scholar 
    Menke, S., Holway, D., Fisher, R. & Jetz, W. Characterizing and predicting species distributions across environments and scales: Argentine ant occurrences in the eye of the beholder. Glob. Ecol. Biogeogr. 18, 50–63 (2009).
    Google Scholar 
    Warren, D. L. & Seifert, S. N. Ecological niche modeling in Maxent: The importance of model complexity and the performance of model selection criteria. Ecol. Appl. 21, 335–342 (2011).PubMed 

    Google Scholar 
    Celenk, S., Dirmenci, T., Malyer, H. & Bicakci, A. A palynological study of the genus Nepeta L.(Lamiaceae). Plant Syst. Evol. 276, 105–123 (2008).
    Google Scholar 
    Zargari, A. Medicinal Plants Vol. 2 (University of Tehran Pub, 1990).
    Google Scholar 
    Javidnia, K., Miri, R., Rezazadeh, S. R., Soltani, M. & Khosravi, A. R. Essential oil composition of two subspecies of Nepeta glomerulosa Boiss. from Iran. Nat. Prod. Commun. 3, 1934578X0800300530 (2008).
    Google Scholar 
    Jamzad, Z. Flora of Iran, no 76, Lamiaceae. Res. Inst. For. Rangel. Tehran 76, 542–544 (2012).
    Google Scholar 
    Talebi, S. M., Nohooji, M. G., Yarmohammadi, M., Azizi, N. & Matsyura, A. Trichomes morphology and density analysis in some Nepeta species of Iran. Mediterr. Bot. 39, 51–62 (2018).
    Google Scholar 
    Amirmohammadi, F., Azizi, M., Nemati, S. H., Memariani, F. & Murphy, R. Nutlet micro‐morphology of selected species of Nepeta (Lamiaceae) in Iran. Nord. J. Bot. (2019).Jamzad, Z., Chase, M. W., Ingrouille, M., Simmonds, M. S. & Jalili, A. Phylogenetic relationships in Nepeta L.(Lamiaceae) and related genera based on ITS sequence data. Taxon 52, 21–32 (2003).
    Google Scholar 
    Emami, S. A., Yazdian, R., Arab, A., Sadeghi, M. & Tayarani-Najaran, Z. Anti-melanogenic activity of different extracts from aerial parts of Nepeta glomeruloasin on murine melanoma B16F10 cells. Iran. J. Pharm. Sci. 13, 61–74 (2017).
    Google Scholar 
    Narimani, R., Moghaddam, M., Ghasemi Pirbalouti, A. & Mojarab, S. Essential oil composition of seven populations belonging to two Nepeta species from Northwestern Iran. Int. J. Food Prop. 20, 2272–2279 (2017).CAS 

    Google Scholar 
    Hosseini, A., Forouzanfar, F. & Rakhshandeh, H. Hypnotic effect of Nepeta glomerulosa on pentobarbital-induced sleep in mice. Jundishapur J. Nat. Pharm. Prod. https://doi.org/10.17795/jjnpp-25063 (2016).Article 

    Google Scholar 
    Layeghhaghighi, M., Hassanpour Asil, M., Abbaszadeh, B., Sefidkon, F. & Matinizadeh, M. Investigation of altitude on morphological traits and essential oil composition of Nepeta pogonosperma Jamzad and Assadi from Alamut region. J. Med. Plants Prod. 6, 35–40 (2017).
    Google Scholar 
    Sefidkon, F. Essential oil of Nepeta glomerulosa Boiss. from Iran. J. Essent. Oil Res. 13, 422–423 (2001).CAS 

    Google Scholar 
    Djamali, M. et al. Application of the global bioclimatic classification to Iran: Implications for understanding the modern vegetation and biogeography. Ecol. Mediterr. 37, 91–114 (2011).
    Google Scholar 
    Djamali, M., Brewer, S., Breckle, S. W. & Jackson, S. T. Climatic determinism in phytogeographic regionalization: a test from the Irano-Turanian region, SW and Central Asia. Flora Morphol. Distrib. Funct. Ecol. Plants 207, 237–249 (2012).
    Google Scholar 
    Aiello-Lammens, M. E., Boria, R. A., Radosavljevic, A., Vilela, B. & Anderson, R. P. spThin: An R package for spatial thinning of species occurrence records for use in ecological niche models. Ecography 38, 541–545 (2015).
    Google Scholar 
    Escobar, L. E., Lira-Noriega, A., Medina-Vogel, G. & Peterson, A. T. Potential for spread of the white-nose fungus (Pseudogymnoascus destructans) in the Americas: Use of Maxent and NicheA to assure strict model transference. Geospat. Health 9, 221–229 (2014).PubMed 

    Google Scholar 
    Valencia-Rodríguez, D., Jiménez-Segura, L., Rogéliz, C. A. & Parra, J. L. Ecological niche modeling as an effective tool to predict the distribution of freshwater organisms: The case of the Sabaleta Brycon henni (Eigenmann, 1913). PLoS ONE 16, e0247876 (2021).PubMed 
    PubMed Central 

    Google Scholar 
    Merow, C., Smith, M. J. & Silander, J. A. Jr. A practical guide to MaxEnt for modeling species’ distributions: What it does, and why inputs and settings matter. Ecography 36, 1058–1069 (2013).
    Google Scholar 
    Peterson, A. T., Cobos, M. E. & Jiménez-García, D. Major challenges for correlational ecological niche model projections to future climate conditions. Ann. N. Y. Acad. Sci. 1429, 66–77 (2018).ADS 
    PubMed 

    Google Scholar 
    Phillips, S. J., Anderson, R. P. & Schapire, R. E. Maximum entropy modeling of species geographic distributions. Ecol. Model. 190, 231–259 (2006).
    Google Scholar 
    Raghavan, R. K., Peterson, A. T., Cobos, M. E., Ganta, R. & Foley, D. Current and future distribution of the lone star tick, Amblyomma americanum (L.)(Acari: Ixodidae) in North America. PLoS ONE 14, e0209082 (2019).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Muscarella, R. et al. ENM eval: An R package for conducting spatially independent evaluations and estimating optimal model complexity for Maxent ecological niche models. Methods Ecol. Evol. 5, 1198–1205 (2014).
    Google Scholar 
    Ramírez Villegas, J. & Jarvis, A. Downscaling global circulation model outputs: The delta method decision and policy analysis Working Paper No. 1 (2010).Liu, C., Newell, G. & White, M. On the selection of thresholds for predicting species occurrence with presence-only data. Ecol. Evol. 6, 337–348 (2016).PubMed 

    Google Scholar 
    Austin, M. Species distribution models and ecological theory: A critical assessment and some possible new approaches. Ecol. Model. 200, 1–19 (2007).
    Google Scholar 
    Rahmanian, S., Pouyan, S., Karami, S. & Pourghasemi, H. R. In Computers in Earth and Environmental Sciences 245–254 (Elsevier, 2022).Rahmanian, S., Pourghasemi, H. R., Pouyan, S. & Karami, S. Habitat potential modelling and mapping of Teucrium polium using machine learning techniques. Environ. Monit. Assess. 193, 1–21 (2021).
    Google Scholar 
    Domroes, M., Kaviani, M. & Schaefer, D. An analysis of regional and intra-annual precipitation variability over Iran using multivariate statistical methods. Theor. Appl. Climatol. 61, 151–159 (1998).ADS 

    Google Scholar 
    Prevéy, J. et al. Greater temperature sensitivity of plant phenology at colder sites: Implications for convergence across northern latitudes. Glob. Change Biol. 23, 2660–2671 (2017).ADS 

    Google Scholar 
    Rousta, I. et al. Impacts of drought on vegetation assessed by vegetation indices and meteorological factors in Afghanistan. Remote Sens. 12, 2433 (2020).ADS 

    Google Scholar 
    Wang, Y. et al. Contrasting effects of temperature and precipitation on vegetation greenness along elevation gradients of the Tibetan Plateau. Remote Sens. 12, 2751 (2020).ADS 

    Google Scholar 
    Zhang, Y. et al. Vegetation change and its relationship with climate factors and elevation on the Tibetan plateau. Int. J. Environ. Res. Public Health 16, 4709 (2019).PubMed Central 

    Google Scholar 
    Vanneste, T. et al. Impact of climate change on alpine vegetation of mountain summits in Norway. Ecol. Res. 32, 579–593 (2017).
    Google Scholar 
    Rodriguez, C., Navarro, T. & El-Keblawy, A. Covariation in diaspore mass and dispersal patterns in three Mediterranean coastal dunes in southern Spain. Turk. J. Bot. 41, 161–170 (2017).
    Google Scholar 
    Zona, S. Fruit and seed dispersal of Salvia L.(Lamiaceae): A review of the evidence. Bot. Rev. 83, 195–212 (2017).
    Google Scholar 
    Ryding, O. Myxocarpy in the Nepetoideae (Lamiaceae) with notes on myxodiaspory in general. Syst. Geogr. Plants 71, 503–514 (2001).
    Google Scholar 
    Tanaka, K., Ogata, K., Mukai, H., Yamawo, A. & Tokuda, M. Adaptive advantage of myrmecochory in the ant-dispersed herb Lamium amplexicaule (Lamiaceae): Predation avoidance through the deterrence of post-dispersal seed predators. PLoS ONE 10, e0133677 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    Ferreira, P. M. et al. Long-term ecological research in southern Brazil grasslands: Effects of grazing exclusion and deferred grazing on plant and arthropod communities. PLoS ONE 15, e0227706 (2020).CAS 
    PubMed 
    PubMed Central 

    Google Scholar  More

  • in

    Towards net-zero phosphorus cities

    C40 Cities. 700+ cities in 53 countries now committed to halve emissions by 2030 and reach net zero by 2050. C40 Cities https://www.c40.org/news/cities-committed-race-to-zero/ (2021).Watts, M. Cities spearhead climate action. Nat. Clim. Change 7, 537–538 (2017).
    Google Scholar 
    Brownlie, W. J. et al. Global actions for a sustainable phosphorus future. Nat. Food 2, 71–74 (2021).CAS 

    Google Scholar 
    El Wali, M., Golroudbary, S. R. & Kraslawski, A. Circular economy for phosphorus supply chain and its impact on social sustainable development goals. Sci. Total Environ. 777, 146060 (2021).CAS 

    Google Scholar 
    Bai, X. et al. Defining and advancing a systems approach for sustainable cities. Curr. Opin. Environ. Sustain. 23, 69–78 (2016).
    Google Scholar 
    De Boer, M. A., Wolzak, L. & Slootweg, J. C. Phosphorus: reserves, production, and applications. in Phosphorus Recovery and Recycling. (eds. Ohtake, H. & Tsuneda, S.) 75–100 (Springer, 2019).Brownlie, W. J. et al. Chapter 2. Phosphorus reserves, resources and uses. In Our Phosphorus Future (eds. Brownlie, W. J., Sutton, M. A., Heal, K. V., Reay, D. S. & Spears, B. M.) (UK Centre for Ecology & Hydrology, 2022). https://doi.org/10.13140/RG.2.2.25016.83209.Chow, E. China issues phosphate quotas to rein in fertiliser exports – analysts. Reuters (2022).Klesty, V. Global food supply at risk from Russian invasion of Ukraine, Yara says. Reuters (2022).Dumas, M., Frossard, E. & Scholz, R. W. Modeling biogeochemical processes of phosphorus for global food supply. Chemosphere 84, 798–805 (2011).CAS 

    Google Scholar 
    Cordell, D., Turner, A. & Chong, J. The hidden cost of phosphate fertilizers: mapping multi-stakeholder supply chain risks and impacts from mine to fork. Glob. Change Peace Secur. 27, 1–21 (2015).
    Google Scholar 
    Metson, G. S., Bennett, E. M. & Elser, J. J. The role of diet in phosphorus demand. Environmental Research Letters 7, 044043 (2012).
    Google Scholar 
    Oita, A., Wirasenjaya, F., Liu, J., Webeck, E. & Matsubae, K. Trends in the food nitrogen and phosphorus footprints for Asia’s giants: China, India, and Japan. Resour. Conserv. Recycl. 157, 104752 (2020).
    Google Scholar 
    Chen, M. & Graedel, T. E. A half-century of global phosphorus flows, stocks, production, consumption, recycling, and environmental impacts. Glob. Environ. Chang. 36, 139–152 (2016).
    Google Scholar 
    Johnes, P. J. et al. Chapter 5. Phosphorus and water quality. in Our Phosphorus Future (eds. Brownlie, W. J., Sutton, M. A., Heal, K. V., Reay, D. S. & Spears, B. M.) (UK Centre for Ecology & Hydrology, 2022). https://doi.org/10.13140/RG.2.2.14950.50246.Dodds, W. K. et al. Eutrophication of US freshwaters: analysis of potential economic damages. Environ. Sci. Technol. 43, 12–19 (2008).
    Google Scholar 
    Watson, S. B. et al. The re-eutrophication of Lake Erie: Harmful algal blooms and hypoxia. Harmful Algae 56, 44–66 (2016).CAS 

    Google Scholar 
    Rabalais, N. N. & Turner, R. E. Gulf of Mexico Hypoxia: Past, Present, and Future. Limnol. Oceanogr. Bull. 28, 117–124 (2019).
    Google Scholar 
    Carstensen, J. & Conley, D. J. Baltic Sea Hypoxia Takes Many Shapes and Sizes. Limnol. Oceanog. Bull. 28, 125–129 (2019).
    Google Scholar 
    Kanter, D. R. & Brownlie, W. J. Joint nitrogen and phosphorus management for sustainable development and climate goals. Environ. Sci. Policy 92, 1–8 (2019).CAS 

    Google Scholar 
    Hamilton, D. P., Salmaso, N. & Paerl, H. W. Mitigating harmful cyanobacterial blooms: strategies for control of nitrogen and phosphorus loads. Aquat. Ecol. 50, 351–366 (2016).CAS 

    Google Scholar 
    Brownlie, W. J. et al. Chapter 9. Towards our phosphorus future. In Our Phosphorus Future (eds. Brownlie, W. J., Sutton, M. A., Heal, K. V., Reay, D. S. & Spears, B. M.) (UK Centre for Ecology & Hydrology, 2022). https://doi.org/10.13140/RG.2.2.16995.22561.MacDonald, G. K. et al. Guiding phosphorus stewardship for multiple ecosystem services. Ecosyst. Health Sustain. 2, e01251 (2016).
    Google Scholar 
    Withers, P. J. A. et al. Stewardship to tackle global phosphorus inefficiency: The case of Europe. Ambio 44, 193–206 (2015).CAS 

    Google Scholar 
    Withers, P. J. A. et al. Towards resolving the phosphorus chaos created by food systems. Ambio 49, 1076–1089 (2020).CAS 

    Google Scholar 
    Withers, P. J. A. Closing the phosphorus cycle. Nat. Sustain. 2, 1001–1002 (2019).
    Google Scholar 
    Langhans, C., Beusen, A. H. W., Mogollón, J. M. & Bouwman, A. F. Phosphorus for Sustainable Development Goal target of doubling smallholder productivity. Nat. Sustain. 5, 57–63 (2022).
    Google Scholar 
    Kuss, P. & Nicholas, K. A. A dozen effective interventions to reduce car use in European cities: Lessons learned from a meta-analysis and transition management. Case Stud. Transp. Policy. 10, 1494–1513 (2022).
    Google Scholar 
    Hobbie, S. E. et al. Contrasting nitrogen and phosphorus budgets in urban watersheds and implications for managing urban water pollution. Proc. Natl. Acad. Sci. USA 114, E4116–E4116 (2017).
    Google Scholar 
    Seto, K. C. et al. From low- to net-zero carbon cities: the next global agenda. Annu. Rev. Environ. Resour. 46, 377–415 (2021).
    Google Scholar 
    Zhang, Y. Urban metabolism: A review of research methodologies. Environ. Pollut. 178, 463–473 (2013).CAS 

    Google Scholar 
    Kissinger, M. & Stossel, Z. An integrated, multi-scale approach for modelling urban metabolism changes as a means for assessing urban sustainability. Sustain. Cities Soc. 67, 102695 (2021).
    Google Scholar 
    Li, H. & Kwan, M.-P. Advancing analytical methods for urban metabolism studies. Resour. Conserv. Recycl. 132, 239–245 (2018).
    Google Scholar 
    Goldstein, B., Birkved, M., Quitzau, M.-B. & Hauschild, M. Quantification of urban metabolism through coupling with the life cycle assessment framework: concept development and case study. Environ. Res. Lett. 8, 035024 (2013).CAS 

    Google Scholar 
    Kovac, A. et al. Global Protocol for Community-Scale Greenhouse Gas Inventories— An Accounting and Reporting Standard for Cities Version 1.1. 190 https://ghgprotocol.org/greenhouse-gas-protocol-accounting-reporting-standard-cities.Rogelj, J., Geden, O., Cowie, A. & Reisinger, A. Net-zero emissions targets are vague: three ways to fix. Nature 591, 365–368 (2021).CAS 

    Google Scholar 
    Wiedmann, T. et al. Three-scope carbon emission inventories of global cities. J. Ind. Ecol. 25, 735–750 (2021).CAS 

    Google Scholar 
    Metson, G. S. et al. Urban phosphorus sustainability: Systemically incorporating social, ecological, and technological factors into phosphorus flow analysis. Environ. Sci. Policy 47, 1–11 (2015).CAS 

    Google Scholar 
    Harseim, L., Sprecher, B. & Zengerling, C. Phosphorus governance within planetary boundaries: the potential of strategic local resource planning in The Hague and Delfland, The Netherlands. Sustainability 13, 10801 (2021).CAS 

    Google Scholar 
    Coutard, O. & Florentin, D. Resource ecologies, urban metabolisms, and the provision of essential services. J. Urban Technol. 29, 49–58 (2022).
    Google Scholar 
    UDG at COP26 | Urban Design Events. Urban Design Group https://www.udg.org.uk/events/2021/udg-cop26 (2021).Ramaswami, A., Russell, A. G., Culligan, P. J., Sharma, K. R. & Kumar, E. Meta-principles for developing smart, sustainable, and healthy cities. Science 352, 940–943 (2016).CAS 

    Google Scholar 
    McPhearson, T. et al. A social-ecological-technological systems framework for urban ecosystem services. One Earth 5, 505–518 (2022).
    Google Scholar 
    McPhearson, T., Haase, D., Kabisch, N. & Gren, Å. Advancing understanding of the complex nature of urban systems. Ecol. Indic. 70, 566–573 (2016).
    Google Scholar 
    Metson, G. S. et al. Socio-environmental consideration of phosphorus flows in the urban sanitation chain of contrasting cities. Regional Environmental Change 18, 1387–1401 (2018).
    Google Scholar 
    Iwaniec, D. M., Metson, G. S. & Cordell, D. P-FUTURES: Towards urban food & water security through collaborative design and impact. Curr. Opin. Environ. Sustain. 20, 1–7 (2016).
    Google Scholar 
    Bulkeley, H. et al. Urban living laboratories: Conducting the experimental city? Eur. Urban. Reg. Stud. 26, 317–335 (2019).
    Google Scholar 
    Beukers, E. & Bertolini, L. Learning for transitions: An experiential learning strategy for urban experiments. Environ. Innov. Soc. Transit. 40, 395–407 (2021).
    Google Scholar 
    Ramaswami, A. et al. Carbon analytics for net-zero emissions sustainable cities. Nat. Sustain. 4, 460–463 (2021).
    Google Scholar 
    Petit-Boix, A., Apul, D., Wiedmann, T. & Leipold, S. Transdisciplinary resource monitoring is essential to prioritize circular economy strategies in cities. Environ. Res. Lett. 17, 021001 (2022).
    Google Scholar 
    WWAP. Wastewater: The Untapped Resource. https://www.unwater.org/publications/un-world-water-development-report-2017 (2017).van Puijenbroek, P. J. T. M., Beusen, A. H. W. & Bouwman, A. F. Global nitrogen and phosphorus in urban waste water based on the Shared Socio-economic pathways. J. Environ. Manage. 231, 446–456 (2019).
    Google Scholar 
    Kovacs, A. & Zavadsky, I. Success and sustainability of nutrient pollution reduction in the Danube River Basin: recovery and future protection of the Black Sea Northwest shelf. Water Int. 46, 176–194 (2021).
    Google Scholar 
    Trimmer, J. T. & Guest, J. S. Recirculation of human-derived nutrients from cities to agriculture across six continents. Nat. Sustain. 1, 427–435 (2018).
    Google Scholar 
    Powers, S. M. et al. Global opportunities to increase agricultural independence through phosphorus recycling. Earths Future 7, 370–383 (2019).
    Google Scholar 
    Metson, G. S., Cordell, D., Ridoutt, B. & Mohr, S. Mapping phosphorus hotspots in Sydney’s organic wastes: a spatially-explicit inventory to facilitate urban phosphorus recycling. J. Urban Ecol. 4, 1–19 (2018).
    Google Scholar 
    Hu, Y., Sampat, A. M., Ruiz-Mercado, G. J. & Zavala, V. M. Logistics Network Management of Livestock Waste for Spatiotemporal Control of Nutrient Pollution in Water Bodies. ACS Sustain. Chem. Eng. 7, 18359–18374 (2019).CAS 

    Google Scholar 
    Mayer, B. K. et al. Total value of phosphorus recovery. Environ. Sci. Technol. 50, 6606–6620 (2016).CAS 

    Google Scholar 
    van Hessen, J. An Assessment of Small-Scale Biodigester Programmes in the Developing World: The SNV and Hivos Approach. (Vrije Universiteit Amsterdam, 2014).Harder, R., Wielemaker, R., Larsen, T. A., Zeeman, G. & Öberg, G. Recycling nutrients contained in human excreta to agriculture: Pathways, processes, and products. Crit. Rev. Environ. Sci. Technol. 49, 695–743 (2019).
    Google Scholar 
    Metson, G. S. et al. Chapter 8. Consumption: the missing link towards phosphorus security. In Our Phosphorus Future (eds. Brownlie, W. J., Sutton, M. A., Heal, K. V., Reay, D. S. & Spears, B. M.) (UK Centre for Ecology & Hydrology, 2022). https://doi.org/10.13140/RG.2.2.36498.73925.Qiao, M., Zheng, Y. M. & Zhu, Y. G. Material flow analysis of phosphorus through food consumption in two megacities in northern China. Chemosphere 84, 773–778 (2011).CAS 

    Google Scholar 
    Forber, K. J., Rothwell, S. A., Metson, G. S., Jarvie, H. P. & Withers, P. J. A. Plant-based diets add to the wastewater phosphorus burden. Environ. Res. Lett. 15, 094018 (2020).CAS 

    Google Scholar 
    UN Population Division. The World’s cities in 2018. https://digitallibrary.un.org/record/3799524 (2018).Klöckner, C. A. A comprehensive model of the psychology of environmental behaviour-A meta-analysis. Glob. Environ. Change 23, 1028–1038 (2013).
    Google Scholar 
    Nyborg, K. et al. Social norms as solutions. Science 354, 42–43 (2016).CAS 

    Google Scholar 
    Vermeir, I. & Verbeke, W. Sustainable Food Consumption: Exploring the Consumer “Attitude – Behavioral Intention” Gap. J. Agric. Environ. Ethics 19, 169–194 (2006).
    Google Scholar 
    Ullström, S., Stripple, J. & Nicholas, K. A. From aspirational luxury to hypermobility to staying on the ground: changing discourses of holiday air travel in Sweden. J. Sustain. Tour. https://doi.org/10.1080/09669582.2021.1998079 (2021).Morris, T. H. Experiential learning—a systematic review and revision of Kolb’s model. Interact. Learn. Environ. 28, 1064–1077 (2020).
    Google Scholar 
    Metson, G. S. & Bennett, E. M. Facilitators & barriers to organic waste and phosphorus re-use in Montreal. Elementa 3, 000070 (2015).
    Google Scholar 
    Winkler, B., Maier, A. & Lewandowski, I. Urban gardening in germany: cultivating a sustainable lifestyle for the societal transition to a bioeconomy. Sustainability 11, 801 (2019).
    Google Scholar 
    Kim, J. E. Fostering behaviour change to encourage low-carbon food consumption through community gardens. Int. J. Urban Sci. 21, 364–384 (2017).
    Google Scholar 
    Fuhr, H., Hickmann, T. & Kern, K. The role of cities in multi-level climate governance: local climate policies and the 1.5 °C target. Curr. Opin. Environ. Sustain. 30, 1–6 (2018).
    Google Scholar 
    Steffen, W. et al. Planetary boundaries: Guiding human development on a changing planet. Science 347, 1259855 (2015).
    Google Scholar 
    Santos, A. F., Almeida, P. V., Alvarenga, P., Gando-Ferreira, L. M. & Quina, M. J. From wastewater to fertilizer products: Alternative paths to mitigate phosphorus demand in European countries. Chemosphere 284, 131258 (2021).CAS 

    Google Scholar 
    UNFCCC. Race To Zero Campaign. https://unfccc.int/climate-action/race-to-zero-campaign.Locsin, J. A., Hood, K. M., Doré, E., Trueman, B. F. & Gagnon, G. A. Colloidal lead in drinking water: Formation, occurrence, and characterization. Crit. Rev. Environ. Sci. Technol. https://doi.org/10.1080/10643389.2022.2039549 (2022).Li, Y. et al. The role of freshwater eutrophication in greenhouse gas emissions: A review. Sci. Total Environ. 768, 144582 (2021).CAS 

    Google Scholar 
    Gong, H. et al. Synergies in sustainable phosphorus use and greenhouse gas emissions mitigation in China: Perspectives from the entire supply chain from fertilizer production to agricultural use. Sci. Total Environ. 838, 155997 (2022).CAS 

    Google Scholar  More