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    Biological and biochemical diversity in different biotypes of spotted stem borer, Chilo partellus (Swinhoe) in India

    1.
    Dujardin, J. P. Aporte de la genetica poblacional al control y vigilancia de vectores de la enfermedad de Chagas. In Curso Posgrado Genética Poblacional de Triatomineos Aplicada al Control Vectorial de la Enfermedad de Chagas (ed. Guhl, F.) 13–15 (Corcas Editores Ltda, 1997).
    Google Scholar 
    2.
    Pires, H. H. R., Barbosa, S. E., Margonari, C., Jurberg, J. & Diotaiuti, L. Variations of the external male genitalia in three populations of Triatoma infestans Klug, 1834. Minist. Saúde 93(4), 479–483 (1998).
    CAS  Google Scholar 

    3.
    Bambou, A. E. et al. Comparing genetic diversity of Sitophilus zeamais(Motchulsky) populations sampled in several agro-ecological areas between Central African Republic and Senegal. South Asian J. Exp. Biol. 4(4), 172–182 (2014).
    Google Scholar 

    4.
    Baldwin, J. D. & Dingle, H. Geographic variation in the effects of temperature on life-history traits in the large milkweed bug Oncopeltus fasciatus. Oecologia 69, 64–71 (1986).
    ADS  Article  Google Scholar 

    5.
    Blanckenhorn, W. U. Altitudinal life history variation in the dung flies Scathophaga stercoraria and Sepsis cynipsea. Oecologia 109, 342–352 (1997).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    6.
    Ikten, C., Skoda, S. R., Hunt, T. E., Molina-Ochoa, J. & Foster, J. E. Genetic variation and inheritance of diapause induction in two distinct voltine ecotypes of Ostrinia nubilalis (Lepidoptera: Crambidae). Ann. Entomol. Soc. Am. 104, 567–575 (2011).
    Article  Google Scholar 

    7.
    Dhillon, M. K., Hasan, F., Tanwar, A. K. & Bhadauriya, A. P. S. Effects of thermo-photoperiod on induction and termination of hibernation in Chilo partellus (Swinhoe). Bull. Entomol. Res. 107, 294–302 (2017).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    8.
    Sharma, H. C. Host plant resistance to insects in sorghum and its role in integrated pest management. Crop Prot. 12, 11–34 (1993).
    Article  Google Scholar 

    9.
    Dhillon, M. K., Hasan, F., Tanwar, A. K. & Bhadauriya, A. P. S. Factors responsible for aestivation in spotted stem borer, Chilo partellus (Swinhoe). J. Exp. Zool. A 331, 326–340 (2019).
    Article  Google Scholar 

    10.
    Dhillon, M. K. & Hasan, F. Consequences of diapause on post-diapause development, reproductive physiology and population growth of Chilo partellus (Swinhoe). Physiol. Entomol. 43, 196–206 (2018).
    CAS  Article  Google Scholar 

    11.
    Dhillon, M. K., Tanwar, A. K. & Hasan, F. Fitness consequences of delayed mating on reproductive performance of Chilo partellus (Swinhoe). J. Exp. Zool. A 331, 161–167 (2019).
    Article  Google Scholar 

    12.
    Dhillon, M. K. et al. Genetic regulation of diapause and associated traits in Chilo partellus (Swinhoe). Sci. Rep. 10, 1793 (2020).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    13.
    Chown, S. L. & Terblanche, J. S. Physiological diversity in insects: Ecological and evolutionary contexts. Adv. Insect Physiol. 33, 50–152 (2006).
    Article  Google Scholar 

    14.
    Sezonlin, M. et al. Phylogeography and population genetics of the maize stalk borer Busseola fusca (Lepidoptera, Noctuidae) in sub-Saharan Africa. Mol. Ecol. 15(2), 407–420 (2006).
    CAS  PubMed  Article  Google Scholar 

    15.
    Rowntree, J. K., Cameron, D. D. & Preziosi, R. F. Genetic variation changes the interactions between the parasitic plant-ecosystem engineer Rhinanthus and its hosts. Philos. Trans. R. Soc. B 366, 1380–1388 (2011).
    Article  Google Scholar 

    16.
    Giron, D. et al. Promises and challenges in insect–plant interactions. Entomol. Exp. Appl. 166(5), 319–343 (2018).
    Article  Google Scholar 

    17.
    Williams, R. S. & Howells, J. M. Effects of intraspecific genetic variation and prior herbivory in an old-field plant on the abundance of the specialist aphid Uroleucon nigrotuberculatum (Hemiptera: Aphididae). Environ. Entomol. 47, 422–431 (2018).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    18.
    Matsubayashi, K. W., Ohshima, I. & Nosil, P. Ecological speciation in phytophagous insects. Entomol. Exp. Appl. 134, 1–27 (2010).
    Article  Google Scholar 

    19.
    Feder, J. L. et al. Allopatric genetic origins for sympatric host-plant shifts and race formation in Rhagoletis. Proc. Natl Acad. Sci USA 100, 10314–10319 (2003).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    20.
    Althoff, M. D. & Pellmyr, O. Examining genetic structure in bogus yucca moth: A sequential approach to phylogeography. Evolution 56, 1632–1643 (2002).
    PubMed  Article  Google Scholar 

    21.
    Knowles, L. L. & Maddison, W. P. Statistical phylogeography. Mol. Ecol. 11, 2623–2635 (2002).
    PubMed  Article  Google Scholar 

    22.
    Templeton, A. R. Statistical phylogeography: Methods of evaluating and minimizing inference errors. Mol. Ecol. 13, 789–809 (2004).
    PubMed  Article  Google Scholar 

    23.
    Thomas, Y., Bethenod, M. T., Pelozuelo, L., Frérot, B. & Bourguet, D. Genetic isolation between two sympatric host-plant races of the European corn borer, Ostrinia nubilalis Hübner. I. Sex pheromone, moth emergence timing, and parasitism. Evolution 57, 261–273 (2003).
    PubMed  Google Scholar 

    24.
    Sharma, H. C., Taneja, S. L., Kameswara Rao, N. & Prasada Rao, K. E. Evaluation of sorghum germplasm for resistance to insect pests. Inf. Bull. 63, 177 (2003).
    Google Scholar 

    25.
    Sharma, H. C., Dhillon, M. K., Pampapathy, G. & Reddy, B. V. S. Inheritance of resistance to spotted stem borer, Chilo partellus in sorghum, Sorghum bicolor. Euphytica 156, 117–128 (2007).
    Article  Google Scholar 

    26.
    Kanta, U., Dhillon, B. S. & Sekhon, S. S. Evaluation and development of maize germplasm for resistance to spotted stem borer. In Insect Resistant Maize: Recent Advances and Utilization (ed. Mihm, J. A.) 246–254 (Proceedings of an International Symposium CIMMYT, 1997).
    Google Scholar 

    27.
    Rakshit, S. et al. Catalogue of Indian maize inbred lines. Tech. Bull. 3, 40 (2008).
    Google Scholar 

    28.
    Agrawal, A. A. Phenotypic plasticity in the interactions and evolution of species. Science 294, 321–326 (2001).
    ADS  CAS  PubMed  Article  Google Scholar 

    29.
    Stireman, J. O. III., Nason, J. D. & Heard, S. B. Host-associated genetic differentiation in phytophagous insects: general phenomenon or isolated exceptions? Evidence from a goldenrod-insect community. Evolution 59, 2573–2587 (2005).
    CAS  PubMed  Article  Google Scholar 

    30.
    Zytynska, S. E. & Preziosi, R. F. Genetic interactions influence host preference and performance in a plant-insect system. Evol. Ecol. 25, 1321–1333 (2011).
    Article  Google Scholar 

    31.
    Zytynska, S. E. & Preziosi, R. F. Host preference of plant genotypes is altered by intraspecific competition in a phytophagous insect. Arthropod-Plant Interact. 7, 349–357 (2013).
    Article  Google Scholar 

    32.
    Sharma, H. C. Biotechnological Approaches for Pest Management and Ecological Sustainability (CRC Press, 2009).
    Google Scholar 

    33.
    Sharma, H. C. & Dhillon, M. K. Climate change effects on arthropod diversity and its implications for pest management and sustainable crop production. In Agroclimatology: Linking Agriculture to Climate (eds Hatfield, J. L. et al.) 595–619 (Crop Science Society of America and Soil Science Society of America Inc, Madison, WI, 2020).
    Google Scholar 

    34.
    Smith, C. M. Plant Resistance to Arthropods: Molecular and Conventional Approaches (Springer, 2005).
    Google Scholar 

    35.
    Dhillon, M. K. & Sharma, H. C. Paradigm shifts in research on host plant resistance to insect pests. Indian J. Plant Protect. 40(1), 1–11 (2012).
    Google Scholar 

    36.
    Funk, D. J. Isolating a role for natural selection in speciation: Host adaptation and sexual isolation in Neochlamisus bebbianae leaf beetles. Evolution 52, 1744–1759 (1998).
    PubMed  Article  PubMed Central  Google Scholar 

    37.
    Dres, M. & Mallet, J. Host races in plant-feeding insects and their importance in sympatric speciation. Philos. Trans. R. Soc. B 357, 471–492 (2002).
    Article  Google Scholar 

    38.
    Rundle, H. D. & Nosil, P. Ecological speciation. Ecol. Lett. 8, 336–352 (2005).
    Article  Google Scholar 

    39.
    Schluter, D. Evidence for ecological speciation and its alternative. Science 323, 737–741 (2009).
    ADS  CAS  PubMed  Article  Google Scholar 

    40.
    Ishiguro, N. & Tsuchida, K. Polymorphic microsatellite loci for the rice stem borer, Chilo suppressalis (Walker) (Lepidoptera: Crambidae). Appl. Entomol. Zool. 41, 565–568 (2006).
    CAS  Article  Google Scholar 

    41.
    Mukhopadhyay, J., Ghosh, K., Rangel, E. F. & Munstermann, L. E. Genetic variability in biochemical characters of Brazilian field populations of the Leishmania vector, Lutzomyia longipalpis (Diptera: Psychodidae). Am. J. Trop. Med. Hyg. 59(6), 893–901 (1998).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    42.
    Vijaya Lakshmi, P., Amudhan, S., Bindu, K. H., Cheralu, C. & Bentur, J. S. A new biotype of the Asian rice gall midge Orseolia oryzae (Diptera: Cecidomyiidae) characterized from the Warangal population in Andhra Pradesh, India. Int. J. Trop. Insect Sci. 26, 207–211 (2006).
    Google Scholar 

    43.
    Himabindu, K., Suneetha, K., Sama, V. S. A. K. & Bentur, J. S. A new rice gall midge resistance gene in the breeding line CR57-MR1523, mapping with flanking markers and development of NILs. Euphytica 174, 179–187 (2010).
    CAS  Article  Google Scholar 

    44.
    Ratcliffe, R. H. et al. Biotype composition of Hessian fly (Diptera: Cecidomyiidae) populations from the Southeastern, Midwestern, and Northwestern United States and virulence to resistance genes in wheat. J. Econ. Entomol. 93(4), 1319–1328 (2000).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    45.
    Zhou, H. et al. Genetic analysis and fine mapping of the gall midge resistance gene Gm5 in rice (Oryza sativa L.). Theor. Appl. Genet. 133, 2021–2033 (2020).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    46.
    Dhillon, M. K. & Kumar, S. Amino acid profiling of Sorghum bicolor vis-à-vis Chilo partellus (Swinhoe) for biochemical interactions and plant resistance. Arthropod-Plant Interact. 11, 537–550 (2017).
    Article  Google Scholar 

    47.
    Dhillon, M. K. & Kumar, S. Lipophilic profiling of Sorghum bicolor (L.) seedlings vis-à-vis Chilo partellus (Swinhoe) larvae reveals involvement of biomarkers in sorghum-stem borer interactions. Indian J. Exp. Biol. 58, 95–108 (2020).
    CAS  Google Scholar 

    48.
    Atray, I., Bentur, J. S. & Nair, S. The Asian rice gall midge (Orseolia oryzae) mitogenome has evolved novel gene boundaries and tandem repeats that distinguish its biotypes. PLoS ONE 10(7), e0134625 (2015).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    49.
    Fujita, D., Kohli, A. & Horgan, F. G. Rice resistance to planthoppers and leafhoppers. Crit. Rev. Plant Sci. 32, 162–191 (2013).
    CAS  Article  Google Scholar 

    50.
    Diehl, R. S. & Bush, G. L. An evolutionary and applied perspective of insect biotypes. Annu. Rev. Entomol. 29, 471–504 (1984).
    Article  Google Scholar 

    51.
    Claridge, M. F. & Den Hollander, J. A biotype concept and its application to insect pests of agriculture. Crop Prot. 2(1), 85–95 (1983).
    Article  Google Scholar 

    52.
    Downie, D. A. Baubles, bangles, and biotypes: A critical review of the use and abuse of the biotype concept. J. Insect Sci. 10, 176 (2010).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    53.
    Perring, T. M. The Bemisia tabaci species complex. Crop Prot. 20, 725–737 (2001).
    Article  Google Scholar 

    54.
    Wenger, J. A. & Michel, A. P. Implementing an evolutionary framework for understanding genetic relationships of phenotypically defined insect biotypes in the invasive soybean aphid (Aphis glycines). Evol. Appl. 6(7), 1041–1053 (2013).
    PubMed  PubMed Central  Article  Google Scholar 

    55.
    Sharma, H. C., Taneja, S. L., Leuschner, K. & Nwanze, K. F. Techniques to screen sorghum for resistance to insect pests. Inf. Bull. 32, 48 (1992).
    Google Scholar 

    56.
    Kumar, S. & Dhillon, M. K. Lipophilic metabolite profiling of maize and sorghum seeds and seedlings, and their pest spotted stem borer larvae: A standardized GC-MS based approach. Indian J. Exp. Biol. 53, 170–176 (2015).
    PubMed  Google Scholar 

    57.
    Dhillon, M. K., Kumar, S. & Gujar, G. T. A common HPLC-PDA method for amino acid analysis in insects and plants. Indian J. Exp. Biol. 52, 73–79 (2014).
    CAS  PubMed  Google Scholar  More

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    The influence of biochar on the content of carbon and the chemical transformations of fallow and grassland humic acids

    Physicochemical and chemical properties of soils and BioC
    The physicochemical and chemical characteristics of the soils and BioC, as well as selected chemical properties of the HAs isolated from the soil and BioC are shown in Table 1.
    Table 1 Physicochemical and chemical characteristics of soils, BioC and isolated HAs.
    Full size table

    The properties of soils and BioC, such as the d, Corg, A, pH, and Q, were presented in detail previously4. Briefly, soils were characterised by a typical d value for mineral soils ≈ 2.60 g cm−3, and by a relatively low content of Corg and a high content of A. The pH of the soils was weakly acidic. The examined soils were characterised by low Q values, indicating a low content of organic structures dissociating to the negative surface charge (mainly carboxylic and phenolic groups). The HAs obtained from fallow and grassland were characterised by high QHA values (about 50 times higher in comparison with the Q values of fallow and grassland). The d value of BioC was typical for organic materials (1.46 g cm−3), moreover, the BioC contained a high content of OM, which was expressed as Corg. The pH of BioC was alkaline. This material was also characterised by a high Q value, which indicated its favourable sorption properties.
    The results of our studies showed that the E2/6 values were similar for the HAs originated from the two studied soils, suggesting a similar ratio of lignin-type compounds resistant to humification to the structures with a high humification degree. The ΔlgK reached values of 0.83 and 0.86 for HAs isolated from grassland and fallow, respectively, indicating a low degree of HA humification (Kumada’s classification for low humification degree of HAs: ΔlgK = 0.8–1.1)33. Slightly higher ΔlgK values obtained for the grassland HAs compared with the fallow suggested a higher content of less humified compounds, such as cellulose, hemicellulose, and lignin34.
    The ΔlgK of HAs isolated from BioC reached a value of 0.54, suggesting the presence of highly humified compounds, in comparison with soil HAs (Kumada’s classification for high humification degree of HAs: ΔlgK  8.0, above which the OH groups are deprotonated26, therefore we only report results in this pH range. Changes in the QHA values as a function of pH (Fig. 4A–D) were monotonic; these values increased towards an alkaline pH, which resulted from the fact that other fractions of functional groups dissociated successively at increasing pH values. Generally, in the first month of the experiment, the highest QHA values were observed for HAs obtained from fallow and grassland with the lowest BioC dose (Fig. 4A,C). This fact indicated that these HAs had the best sorption properties. In the last month of the experiment, the QHA values changed in an ambiguous way. The QHA at pH 9.0 values of HAs isolated from pure BioC were lower than those obtained from the soil, and moreover, BioC did not have an obvious effect on the QHA values of the soil HAs. Previous studies4 on impact of BioC on the physicochemical properties of Haplic Luvisol under different land uses, showed that BioC added to soil caused a significant increase in Q values in the last year of the experiment. Thus, we can conclude that BioC introduced OM with a variable surface charge but did not affect the soil’s QHA. It is possible that the BioC doses used in our experiment were insufficient to raise the QHA values.
    Figure 4

    Dependence of surface negative charge (QHA) on pH of the HAs solution. HAs obtained from fallow (A,B) and grassland (C,D) amended with BioC in 1st and 28th month of field experiment, as well as HAs obtained from BioC.

    Full size image

    Influence of BioC amendment on structure and chemical properties of HAs in fallow and grassland: spectroscopic approach
    The analyses of the HAs isolated from fallow and grassland amended with BioC showed changes in the structural properties of these compounds. The E2/6 parameter estimated from UV–Vis data was changing both under the influence of different BioC doses and during the 3 years of the experiment. However, it should be assumed that the observed changes were of a different nature for fallow (Fig. 5A) and for grassland (Fig. 5B), due to varied trends in the activity of BioC on the analysed soils.
    Figure 5

    Changes in E2/6 values obtained for HAs of fallow (A) and grassland (B) amended with BioC (0, 1, 2, 3 kg m−2) as a function of time. Average values from 3 replicates in each term, ± standard deviation. Other letter designations indicate significant differences between values at α  More

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    Tracking late Pleistocene Neandertals on the Iberian coast

    1.
    Bennett, M. R. & Morse, S. A. Human Footprints: Fossilised Locomotion? (Springer International Publishing, Berlin, 2014).
    Google Scholar 
    2.
    Leakey, M. D. & Hay, R. L. Pliocene footprints in the Laetolil Beds at Laetoli, northern Tanzania. Nature 278, 317–323 (1979).
    ADS  Article  Google Scholar 

    3.
    Mietto, P., Avanzini, M. & Rolandi, G. Palaeontology: Human footprints in Pleistocene volcanic ash. Nature 422, 133 (2003).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    4.
    Ashton, N. et al. Hominin footprints from early Pleistocene deposits at Happisburgh, UK. PLoS ONE 9, e88329 (2014).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    5.
    Duveau, J. et al. The composition of a Neandertal social group revealed by the hominin footprints at Le Rozel (Normandy, France). PNAS 116, 19409–19414 (2019).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    6.
    Masao, F. T. et al. New footprints from Laetoli (Tanzania) provide evidence for marked body size variation in early hominins. eLife 5, e19568 (2016).
    PubMed  PubMed Central  Article  Google Scholar 

    7.
    Altamura, F. et al. Archaeology and ichnology at Gombore II-2, Melka Kunture, Ethiopia: Everyday life of a mixed-age hominin group 700,000 years ago. Sci. Rep. 8, 2815 (2018).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    8.
    Bustos, D. et al. Footprints preserve terminal Pleistocene hunt? Human-sloth interactions in North America. Sci. Adv. 4, eaar7621 (2018).
    ADS  PubMed  PubMed Central  Article  Google Scholar 

    9.
    Stewart, M. et al. Human footprints provide snapshot of last interglacial ecology in the Arabian interior. Sci. Adv. 6, eaba8940 (2020).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    10.
    Barton, C. M. Stone tools and paleolithic settlement in the Iberian Peninsula. Proc. Prehist. Soc. 56, 15–32 (1990).
    Article  Google Scholar 

    11.
    Garralda, M. D. The Neandertals from the Iberian Peninsula. MUNIBE 57, 289–314 (2005).
    Google Scholar 

    12.
    Ruiz, M. N. et al. Last Neandertal occupations at Central Iberia: The lithic industry of Jarama VI rock shelter (Valdesotos, Guadalajara, Spain). Archaeol. Anthropol. Sci. 12, 45 (2020).
    Article  Google Scholar 

    13.
    Muñiz, F. et al. Following the last Neandertals: Mammal tracks in Late Pleistocene coastal dunes of Gibraltar (S Iberian Peninsula). Quat. Sci. Rev. 217, 297–309 (2019).
    ADS  Article  Google Scholar 

    14.
    Neto de Carvalho, C. et al. First vertebrate tracks and palaeoenvironment in a MIS-5 context in the Doñana National Park (Huelva, SW Spain). Quat. Sci. Rev. 243, 106508 (2020).
    Article  Google Scholar 

    15.
    Neto de Carvalho, C. et al. Paleoecological implications of large-sized wild boar tracks recorded during the last interglacial (Mis 5) at Huelva (Sw Spain). Palaios 35, 512–523 (2020).
    ADS  Article  Google Scholar 

    16.
    Rodríguez-Ramírez, A. et al. The role of neo-tectonics in the sedimentary infilling and geomorphological evolution of the Guadalquivir estuary (Gulf of Cadiz, SW Spain) during the Holocene. Geomorphology 219, 126–140 (2014).
    ADS  Article  Google Scholar 

    17.
    Rodríguez-Rámirez, A. Geomorfología del Parque Nacional de Doñana y su Entorno. (ed Organismo Autónomo Parques Nacionales) (Ministerio de Medio Ambiente, Madrid, 1998).

    18.
    Pérez Muñoz, A. B. et al. Parque Nacional de Doñana. Guía Geológica. (ed Rodríguez Fernández, R.) (Instituto Geológico y Minero de España & Organismo Autónomo Parques Nacionales, Madrid, 2020).

    19.
    Instituto Hidrográfico de la Marina. Derrotero N° 2-Tomo 2 (Costas de Portugal y SO de España, Cádiz, 1992).
    Google Scholar 

    20.
    Rodríguez-Ramírez, A. et al. Analysis of the recent storm record in the southwestern spanish coast: Implications for littoral management. Sci. Total Environ. 303, 189–201 (2003).
    ADS  PubMed  Article  CAS  PubMed Central  Google Scholar 

    21.
    Gibbard, P. L., Head, M. J., Walker, M. J. C. & The Subcommission on Quaternary Stratigraphy. Formal ratification of the Quaternary System/Period and the Pleistocene Series/Epoch with a base at 2.58 Ma. J. Quat. Sci. 25, 96–102 (2010).
    Article  Google Scholar 

    22.
    Zazo, C. et al. Landscape evolution and geodynamic controls in the Gulf of Cadiz (Huelva coast, SW Spain) during the Late Quaternary. Geomorphology 68, 269–290 (2005).
    ADS  Article  Google Scholar 

    23.
    Duveau, J. Les empreintes de pieds du Rozel (Manche). Instantanés de groupes humains au Pléistocène supérieur. Approche combinée morphométrique et expérimentale. (Ph. D. dissertation. Muséum national d’Histoire naturelle, Paris, 2020).

    24.
    Manolis, S., Aiello, L., Henessy, R., Kyparissi-Apostolika, N. Middle Palaeolithic Footprints from Theopetra Cave (Thessaly, Greece) (ed Kyparissi-Apostolika, N.) 87–93 (Greek Ministry of Culture and Institute for Aegean Prehistory, Athens, 2000).

    25.
    Onac, B. P. et al. U-Th ages constraining the Neanderthal footprint at Vârtop Cave, Romania. Quat. Sci. Rev. 24, 1151–1157 (2005).
    ADS  Article  Google Scholar 

    26.
    Duveau, J., Berillon, G., Verna, C. 11-On the tracks of Neandertals: The ichnological assemblage from Le Rozel (Normandy, France). (eds Pastoors, A. & Lenssen-Erz, T.) (Springer Nature, in Press).

    27.
    Citton, P., Romano, M., Salvador, I. & Avanzini, M. Reviewing the upper Pleistocene human footprints from the ‘Sala dei Misteri’in the Grotta della Basura (Toirano, northern Italy) cave: An integrated morphometric and morpho-classificatory approach. Quat. Sci. Rev. 169, 50–64 (2017).
    ADS  Article  Google Scholar 

    28.
    Helm, C. W. et al. A New Pleistocene Hominin Tracksite from the Cape South Coast, South Africa. Sci. Rep. 8, 3772 (2018).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    29.
    Dingwall, H. L., Hatala, K. G., Wunderlich, R. E. & Richmond, B. G. Hominin stature, body mass, and walking speed estimates based on 1.5 million-year-old fossil footprints at Ileret, Kenya. J. Hum. Evol. 64, 556–568 (2013).
    PubMed  Article  PubMed Central  Google Scholar 

    30.
    Krishan, K. Estimation of stature from footprint and foot outline dimensions in Gujjars of North India. Forensic Sci. Int. 175, 93–101 (2008).
    PubMed  Article  PubMed Central  Google Scholar 

    31.
    Fawzy, I. A. & Kamal, N. N. Stature and body weight estimation from various footprint measurements among Egyptian population. J. Forensic Sci. 55, 884–888 (2010).
    PubMed  Article  PubMed Central  Google Scholar 

    32.
    Reel, S., Rouse, S., Obe, W. V. & Doherty, P. Estimation of stature from static and dynamic footprints. Forensic Sci. Int. 219, 283-e1 (2012).
    PubMed  Article  PubMed Central  Google Scholar 

    33.
    Hemy, N., Flavel, A., Ishak, N. I. & Franklin, D. Sex estimation using anthropometry of feet and footprints in a Western Australian population. Forensic Sci. Int. 231, 402-e1 (2013).
    PubMed  Article  PubMed Central  Google Scholar 

    34.
    Aiello, L. & Dean, C. An Introduction to Human Evolutionary Anatomy (Academic Press Inc., London, 1990).
    Google Scholar 

    35.
    Klenerman, L. & Wood, B. The Human Foot: A Companion to Clinical Studies (Springer, London, 2006).
    Google Scholar 

    36.
    Elftman, H. & Manter, J. Chimpanzee and human feet in bipedal walking. Am. J. Phys. Anthropol. 20, 69–79 (1935).
    Article  Google Scholar 

    37.
    Alexander, R. M. Principles of Animal Locomotion (Princeton University Press, Princeton, 2003).
    Google Scholar 

    38.
    Ruff, C. B., Trinkaus, E. & Holliday, T. W. Body mass and encephalization in Pleistocene Homo. Nature 387, 173 (1997).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    39.
    Carretero, J. M. et al. Stature estimation from complete long bones in the Middle Pleistocene humans from the Sima de los Huesos, Sierra de Atapuerca (Spain). J. Hum. Evol. 62, 242–255 (2012).
    PubMed  Article  PubMed Central  Google Scholar 

    40.
    Benazzi, S. et al. Early dispersal of modern humans in Europe and implications for Neandertal behaviour. Nature 479, 525–528 (2011).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    41.
    Hublin, J. J. The modern human colonization of western Eurasia: When and where?. Quat. Sci. Rev. 118, 194–210 (2015).
    ADS  Article  Google Scholar 

    42.
    Karavanić, I. et al. Paleolithic hominins and settlement in Croatia from MIS 6 to MIS 3: Research history and current interpretations. Quat. Int. 494, 152–166 (2018).
    Article  Google Scholar 

    43.
    Vallespi, E., Alvarez, G., Perez Sindreu, F. & Rufete, P. Nuevas atribuciones onubenses al Paleolitico Inferior y Medio. Huelva en su Historia I, 43–56 (1986).

    44.
    Viehmann, I. Prehistoric Human Footprints in Romania’s Caves. Theor. Appl. Karstol. 3, 229–234 (1987).
    Google Scholar 

    45.
    Harvati, K. The human fossil record from Romania: Early Upper Paleolithic European Mandibles and Neanderthal. (eds Harvati, K. & Roksandic, M.) 51–68 (Springer Netherlands, 2016).

    46.
    Zazo, C. et al. Pleistocene and Holocene Aeolian facies along the Huelva coast (southern Spain): Climatic and neotectonic implications. Geol. Mijn. 77, 209–224 (1999).
    Article  Google Scholar 

    47.
    Zazo, C. et al. El complejo eólico de El Abalario (Huelva) (eds Sanjaume, E., Gracia, F. J.) 407–425 (Sociedad Española de Geomorfología, Madrid, 2011)

    48.
    Paerl, H. W. & Yanarell, A. C. Environmental dynamics, community structure and function in a hypersaline microbial mat (eds Seckbach, J. & Oren, A.) 421–442, (Springer Netherlands, 2010).

    49.
    Porada, H. & Bouougri, E. Wrinkle structures—a critical review (eds Schieber, J. et al.) 135–144 (Elsevier, 2007).

    50.
    Gerdes, G. What Are Microbial Mats? (eds Seckbach, J. & Oren, A.) 3–25, (Springer Netherlands, 2010).

    51.
    Eriksson, P. G. et al. Paleoenvironmental Context Of Microbial Mat-Related Structures In Siliciclastic Rocks. (eds Seckbach, J. & Oren, A.) 71–108 (Springer Netherlands, 2010).

    52.
    Zilhão, J. et al. Last Interglacial Iberian Neandertals as fisher-hunter-gatherers. Science 367, 1443 (2020).
    ADS  Article  CAS  Google Scholar 

    53.
    Hardy, B. L. & Moncel, M.-H. Neanderthal use of fish, mammals, birds, starchy plants and wood 125–250,000 years ago. PLoS ONE 6, e23768 (2011).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    54.
    Wall-Scheffler, C. M., Wagnild, J. & Wagler, E. Human footprint variation while performing load bearing tasks. PLoS ONE 10, e0118619 (2015).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    55.
    Romagnoli, F., Martini, F. & Sarti, L. Neanderthal use of Callista chione shells as raw material for retouched tools in South-East Italy: Analysis of Grotta del Cavallo layer l assemblage with a new methodology. J. Archaeol. Method Theory 22, 1007–1037 (2015).
    Article  Google Scholar 

    56.
    Benito, B. M. et al. The ecological niche and distribution of Neanderthals during the Last Interglacial. J. Biogeogr. 44, 51–61 (2017).
    Article  Google Scholar 

    57.
    Villa, P. et al. Neandertals on the beach: Use of marine resources at Grotta dei Moscerini (Latium, Italy). PLoS ONE 15, e0226690 (2020).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    58.
    Cortés-Sánchez, M. et al. Shellfish collection on the westernmost Mediterranean, Bajondillo cave (~ 160–35 cal kyr BP): A case of behavioral convergence?. Quat. Sci. Rev. 217, 284–196 (2019).
    ADS  Article  Google Scholar 

    59.
    Stringer, C. B. et al. Neandertal exploitation of marine mammals in Gibraltar. PNAS 105, 14319–14324 (2008).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar  More

  • in

    Eco-evolutionary interaction between microbiome presence and rapid biofilm evolution determines plant host fitness

    1.
    Slobodkin, L. B. Growth and regulation of animal populations (Holt, Rinehart and Winston, 1961).
    2.
    Thompson, J. N. Rapid evolution as an ecological process. Trends Ecol. Evol. 13, 329–332 (1998).
    CAS  PubMed  Article  Google Scholar 

    3.
    Hendry, A. P. A critique for eco-evolutionary dynamics. Funct. Ecol. 33, 84–94 (2019).
    Article  Google Scholar 

    4.
    Turcotte, M. M., Reznick, D. N. & Hare, J. D. The impact of rapid evolution on population dynamics in the wild: experimental test of eco-evolutionary dynamics. Ecol. Lett. 14, 1084–1092 (2011).
    PubMed  Article  Google Scholar 

    5.
    Hairston, N. G. Jr, Ellner, S. P., Geber, M. A., Yoshida, T. & Fox, J. A. Rapid evolution and the convergence of ecological and evolutionary time. Ecol. Lett. 8, 1114–1127 (2005).
    Article  Google Scholar 

    6.
    Tan, J., Rattray, J. B., Yang, X. & Jiang, L. Spatial storage effect promotes biodiversity during adaptive radiation. Proc. R. Soc. Lond. B 284, 20170841 (2017).
    Google Scholar 

    7.
    Hart, S. P., Turcotte, M. M. & Levine, J. M. Effects of rapid evolution on species coexistence. Proc. Natl Acad. Sci. USA 116, 2112–2117 (2019).
    CAS  PubMed  Article  Google Scholar 

    8.
    Faillace, C. A. & Morin, P. J. Evolution alters the consequences of invasions in experimental communities. Nat. Ecol. Evol. 1, 0013 (2017).
    Article  Google Scholar 

    9.
    Vanbergen, A. J., Espíndola, A. & Aizen, M. A. Risks to pollinators and pollination from invasive alien species. Nat. Ecol. Evol. 2, 16–25 (2018).
    PubMed  Article  Google Scholar 

    10.
    Hendry, A. P. Eco-evolutionary dynamics (Princeton Univ. Press, 2016).

    11.
    Garud, N. R., Good, B. H., Hallatschek, O. & Pollard, K. S. Evolutionary dynamics of bacteria in the gut microbiome within and across hosts. PLoS Biol. 17, e3000102 (2019).
    PubMed  PubMed Central  Article  Google Scholar 

    12.
    Zhao, S. et al. Adaptive evolution within gut microbiomes of healthy people. Cell Host Microbe 25, 656–667 (2019).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    13.
    terHorst, C. P. & Zee, P. C. Eco-evolutionary dynamics in plant–soil feedbacks. Funct. Ecol. 30, 1062–1072 (2016).
    Article  Google Scholar 

    14.
    Soto, M. J., Domínguez‐Ferreras, A., Pérez‐Mendoza, D., Sanjuán, J. & Olivares, J. Mutualism versus pathogenesis: the give‐and‐take in plant–bacteria interactions. Cell. Microbiol. 11, 381–388 (2009).
    CAS  PubMed  Article  Google Scholar 

    15.
    Marchetti, M. et al. Experimental evolution of a plant pathogen into a legume symbiont. PLoS Biol. 8, e1000280 (2010).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    16.
    Saikkonen, K., Wäli, P., Helander, M. & Faeth, S. H. Evolution of endophyte–plant symbioses. Trends Plant Sci. 9, 275–280 (2004).
    CAS  PubMed  Article  Google Scholar 

    17.
    Reese, A. T. & Dunn, R. R. Drivers of microbiome biodiversity: a review of general rules, feces, and ignorance. mBio 9, e01294-18 (2018).
    PubMed  PubMed Central  Article  Google Scholar 

    18.
    Miller, E. T., Svanbäck, R. & Bohannan, B. J. Microbiomes as metacommunities: understanding host-associated microbes through metacommunity ecology. Trends Ecol. Evol. 33, 926–935 (2018).
    PubMed  Article  Google Scholar 

    19.
    Griffin, E. A. et al. Plant host identity and soil macronutrients explain little variation in sapling endophyte community composition: is disturbance an alternative explanation? J. Ecol. 107, 1876–1889 (2019).
    CAS  Article  Google Scholar 

    20.
    Acosta, K. et al. Duckweed hosts a taxonomically similar bacterial assemblage as the terrestrial leaf microbiome. PLoS ONE 15, e0228560 (2020).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    21.
    Sandler, G., Bartkowska, M., Agrawal, A. F. & Wright, S. I. Estimation of the SNP mutation rate in two vegetatively propagating species of duckweed. G3 10, 4191–4200 (2020).
    PubMed  Article  Google Scholar 

    22.
    Ishizawa, H., Kuroda, M., Morikawa, M. & Ike, M. Evaluation of environmental bacterial communities as a factor affecting the growth of duckweed Lemna minor. Biotechnol. Biofuels 10, 62 (2017).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    23.
    Zhang, Y. et al. Duckweed (Lemna minor) as a model plant system for the study of human microbial pathogenesis. PLoS ONE 5, e13527 (2010).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    24.
    Rainey, P. B. & Travisano, M. Adaptive radiation in a heterogeneous environment. Nature 394, 69–72 (1998).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    25.
    Tan, J., Yang, X., He, Q., Hua, X. & Jiang, L. Earlier parasite arrival reduces the repeatability of host adaptive radiation. ISME J. 14, 2358–2360 (2020).
    PubMed  PubMed Central  Article  Google Scholar 

    26.
    Tan, J., Yang, X. & Jiang, L. Species ecological similarity modulates the importance of colonization history for adaptive radiation. Evolution 71, 1719–1727 (2017).
    PubMed  Article  Google Scholar 

    27.
    Meyer, J. R., Schoustra, S. E., Lachapelle, J. & Kassen, R. Overshooting dynamics in a model adaptive radiation. Proc. R. Soc. Lond. B 278, 392–398 (2011).
    Google Scholar 

    28.
    Tan, J., Kelly, C. K. & Jiang, L. Temporal niche promotes biodiversity during adaptive radiation. Nat. Commun. 4, 2102 (2013).
    PubMed  Article  CAS  Google Scholar 

    29.
    Spiers, A. J., Buckling, A. & Rainey, P. B. The causes of Pseudomonas diversity. Microbiology 146, 2345–2350 (2000).
    CAS  PubMed  Article  Google Scholar 

    30.
    Spiers, A. J., Bohannon, J., Gehrig, S. M. & Rainey, P. B. Biofilm formation at the air–liquid interface by the Pseudomonas fluorescens SBW25 wrinkly spreader requires an acetylated form of cellulose. Mol. Microbiol. 50, 15–27 (2003).
    CAS  PubMed  Article  Google Scholar 

    31.
    Bantinaki, E. et al. Adaptive divergence in experimental populations of Pseudomonas fluorescens. III. Mutational origins of wrinkly spreader diversity. Genetics 176, 441–453 (2007).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    32.
    McDonald, M. J., Gehrig, S. M., Meintjes, P. L., Zhang, X.-X. & Rainey, P. B. Adaptive divergence in experimental populations of Pseudomonas fluorescens. IV. Genetic constraints guide evolutionary trajectories in a parallel adaptive radiation. GENETICS 183, 1041–1053 (2009).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    33.
    Bailey, S. F., Dettman, J. R., Rainey, P. B. & Kassen, R. Competition both drives and impedes diversification in a model adaptive radiation. Proc. R. Soc. Lond. B 280, 20131253 (2013).
    Google Scholar 

    34.
    Hansen, S. K., Rainey, P. B., Haagensen, J. A. & Molin, S. Evolution of species interactions in a biofilm community. Nature 445, 533–536 (2007).
    CAS  PubMed  Article  Google Scholar 

    35.
    Flemming, H.-C. et al. Biofilms: an emergent form of bacterial life. Nat. Rev. Microbiol. 14, 563–575 (2016).
    CAS  PubMed  Article  Google Scholar 

    36.
    Ahmad, F., Ahmad, I. & Khan, M. S. Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol. Res. 163, 173–181 (2008).
    CAS  PubMed  Article  Google Scholar 

    37.
    El-Sayed, W. S., Akhkha, A., El-Naggar, M. Y. & Elbadry, M. In vitro antagonistic activity, plant growth promoting traits and phylogenetic affiliation of rhizobacteria associated with wild plants grown in arid soil. Front. Microbiol. 5, 651 (2014).
    PubMed  PubMed Central  Article  Google Scholar 

    38.
    Gómez, P. & Buckling, A. Real-time microbial adaptive diversification in soil. Ecol. Lett. 16, 650–655 (2013).
    PubMed  Article  Google Scholar 

    39.
    Spor, A., Koren, O. & Ley, R. Unravelling the effects of the environment and host genotype on the gut microbiome. Nat. Rev. Microbiol. 9, 279–290 (2011).
    CAS  PubMed  Article  Google Scholar 

    40.
    Walters, W. A. et al. Large-scale replicated field study of maize rhizosphere identifies heritable microbes. Proc. Natl Acad. Sci. USA 115, 7368–7373 (2018).
    PubMed  PubMed Central  Article  Google Scholar 

    41.
    Veach, A. M. et al. Rhizosphere microbiomes diverge among Populus trichocarpa plant-host genotypes and chemotypes, but it depends on soil origin. Microbiome 7, 76 (2019).
    PubMed  PubMed Central  Article  Google Scholar 

    42.
    Lennon, J. T. & Martiny, J. B. Rapid evolution buffers ecosystem impacts of viruses in a microbial food web. Ecol. Lett. 11, 1178–1188 (2008).
    PubMed  Article  Google Scholar 

    43.
    Pantel, J. H., Duvivier, C. & Meester, L. D. Rapid local adaptation mediates zooplankton community assembly in experimental mesocosms. Ecol. Lett. 18, 992–1000 (2015).
    PubMed  Article  Google Scholar 

    44.
    Faillace, C. A. & Morin, P. J. Evolution alters post-invasion temporal dynamics in experimental communities. J. Anim. Ecol. 89, 285–298 (2020).
    PubMed  Article  Google Scholar 

    45.
    Omilian, A. R., Cristescu, M. E. A., Dudycha, J. L. & Lynch, M. Ameiotic recombination in asexual lineages of Daphnia. Proc. Natl Acad. Sci. USA 103, 18638–18643 (2006).
    CAS  PubMed  Article  Google Scholar 

    46.
    Mao, Y., Botella, J. R., Liu, Y. & Zhu, J.-K. Gene editing in plants: progress and challenges. Natl Sci. Rev. 6, 421–437 (2019).
    CAS  Article  Google Scholar 

    47.
    Horvath, P. & Barrangou, R. CRISPR/Cas, the immune system of Bacteria and Archaea. Science 327, 167–170 (2010).
    CAS  PubMed  Article  Google Scholar 

    48.
    Yang, L. et al. Promotion of plant growth and in situ degradation of phenol by an engineered Pseudomonas fluorescens strain in different contaminated environments. Soil Biol. Biochem. 43, 915–922 (2011).
    CAS  Article  Google Scholar 

    49.
    Zabłocka-Godlewska, E., Przystaś, W. & Grabińska-Sota, E. Decolourization of diazo Evans blue by two strains of Pseudomonas fluorescens isolated from different wastewater treatment plants. Water Air Soil Pollut. 223, 5259–5266 (2012).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    50.
    Paulsen, I. T. et al. Complete genome sequence of the plant commensal Pseudomonas fluorescens Pf-5. Nat. Biotechnol. 23, 873–878 (2005).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    51.
    Rainey, P. B. Adaptation of Pseudomonas fluorescens to the plant rhizosphere. Environ. Microbiol. 1, 243–257 (1999).
    CAS  PubMed  Article  Google Scholar 

    52.
    Gilbert, S. et al. Bacterial production of indole related compounds reveals their role in association between duckweeds and endophytes. Front. Chem. 6, 265 (2018).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    53.
    Bailey, M. J., Lilley, A. K., Thompson, I. P., Rainey, P. B. & Ellis, R. J. Site directed chromosomal marking of a fluorescent pseudomonad isolated from the phytosphere of sugar beet; stability and potential for marker gene transfer. Mol. Ecol. 4, 755–764 (1995).
    CAS  PubMed  Article  Google Scholar 

    54.
    Spiers, A. J. & Rainey, P. B. The Pseudomonas fluorescens SBW25 wrinkly spreader biofilm requires attachment factor, cellulose fibre and LPS interactions to maintain strength and integrity. Microbiology 151, 2829–2839 (2005).
    CAS  PubMed  Article  Google Scholar 

    55.
    Lind, P. A., Libby, E., Herzog, J. & Rainey, P. B. Predicting mutational routes to new adaptive phenotypes. eLife 8, e38822 (2019).
    PubMed  PubMed Central  Article  Google Scholar 

    56.
    O’Brien, P. A., Webster, N. S., Miller, D. J. & Bourne, D. G. Host–microbe coevolution: applying evidence from model systems to complex marine invertebrate holobionts. mBio 10, e02241-18 (2019).
    PubMed  PubMed Central  Article  Google Scholar 

    57.
    Theis, K. R. et al. Getting the hologenome concept right: an eco-evolutionary framework for hosts and their microbiomes. mSystems 1, e00028-16 (2016).
    PubMed  PubMed Central  Article  Google Scholar 

    58.
    Landolt, E. Biosystematic Investigations in the Family of Duckweeds (Lemnaceae), Volume 2. The Family of Lemnaceae, A Monographic Study, Volume 1 (Geobotanical Institute, ETH Zurich, 1986).

    59.
    Ziegler, P., Sree, K. S. & Appenroth, K.-J. Duckweeds for water remediation and toxicity testing. Toxicol. Environ. Chem. 98, 1127–1154 (2016).
    CAS  Article  Google Scholar  More

  • in

    Urbanization can benefit agricultural production with large-scale farming in China

    1.
    Gu, B., Zhang, X., Bai, X., Fu, B. & Chen, D. Four steps to food security for swelling cities. Nature 566, 31–33 (2019).
    ADS  CAS  Article  Google Scholar 
    2.
    Godfray, H. C. et al. Food security: the challenge of feeding 9 billion people. Science 327, 812–818 (2010).
    ADS  CAS  Article  Google Scholar 

    3.
    Bren D Amour, C. et al. Future urban land expansion and implications for global croplands. Proc. Natl Acad. Sci. USA 114, 8939–8944 (2017).
    Article  Google Scholar 

    4.
    Gardi, C., Panagos, P., Van Liedekerke, M., Bosco, C. & De Brogniez, D. Land take and food security: assessment of land take on the agricultural production in Europe. J. Environ Plann. Manag. 58, 898–912 (2015).
    Article  Google Scholar 

    5.
    Shi, K. et al. Urban expansion and agricultural land loss in China: a multiscale perspective. Sustainability 8, 790 (2016).
    Article  Google Scholar 

    6.
    Bai, X., Shi, P. & Liu, Y. Society: realizing China’s urban dream. Nature 509, 158–160 (2014).
    Article  Google Scholar 

    7.
    World Urbanization Prospects 2018 (United Nations, 2018); https://population.un.org/wup/Download/

    8.
    Zhai, Z., Chen, J. & Li, L. Future trends of China’s population and aging from 2015 to 2100 [in Chinese]. Popul. Res. 41, 60–71 (2017).
    Google Scholar 

    9.
    Van Vliet, J., Eitelberg, D. A. & Verburg, P. H. A global analysis of land take in cropland areas and production displacement from urbanization. Glob. Environ. Change 43, 107–115 (2017).
    Article  Google Scholar 

    10.
    Chen, J. Rapid urbanization in China: a real challenge to soil protection and food security. Catena 69, 1–15 (2007).
    Article  Google Scholar 

    11.
    Martellozzo, F. et al. Urbanization and the loss of prime farmland: a case study in the Calgary–Edmonton corridor of Alberta. Reg. Environ. Change 15, 881–893 (2015).
    Article  Google Scholar 

    12.
    Yan, H., Liu, J., He, Q. H., Bo, T. & Cao, M. Assessing the consequence of land use change on agricultural productivity in China. Glob. Planet. Change 67, 13–19 (2009).
    ADS  Article  Google Scholar 

    13.
    Bai, X., Chen, J. & Shi, P. Landscape urbanization and economic growth in China: positive feedbacks and sustainability dilemmas. Environ. Sci. Technol. 46, 132–139 (2012).
    ADS  CAS  Article  Google Scholar 

    14.
    Statistical yearbooks of prefecture-level cities in 2015 [in Chinese]. National Bureau of Statistics http://www.stats.gov.cn/tjsj/ (2016).

    15.
    Zuo, L. et al. Progress towards sustainable intensification in China challenged by land-use change. Nat. Sustain. 1, 304–313 (2018).
    Article  Google Scholar 

    16.
    Lal, R. Soil carbon sequestration impacts on global climate change and food security. Science 304, 1623–1627 (2004).
    ADS  CAS  Article  Google Scholar 

    17.
    Zhang, X. et al. Effects of enhancing soil organic carbon sequestration in the topsoil by fertilization on crop productivity and stability: evidence from long-term experiments with wheat–maize cropping systems in China. Sci. Total Environ. 562, 247–259 (2016).
    ADS  CAS  Article  Google Scholar 

    18.
    Wu, Y. et al. Policy distortions, farm size, and the overuse of agricultural chemicals in China. Proc. Natl Acad. Sci. USA 115, 7010–7015 (2018).
    ADS  CAS  Article  Google Scholar 

    19.
    Zou, B., Mishra, A. K. & Luo, B. Aging population, farm succession, and farmland usage: evidence from rural China. Land Use Policy 77, 437–445 (2018).
    Article  Google Scholar 

    20.
    Guidance on Accelerating the Development of Agricultural Productive Services (Ministry of Agriculture and Rural Affairs of the People’s Republic of China, 2017).

    21.
    Ju, X., Gu, B., Wu, Y. & Galloway, J. N. Reducing China’s fertilizer use by increasing farm size. Glob. Environ. Change 41, 26–32 (2016).
    Article  Google Scholar 

    22.
    Ren, C. et al. The impact of farm size on agricultural sustainability. J. Clean Prod. 220, 357–367 (2019).
    Article  Google Scholar 

    23.
    Adamopoulos, T. & Restuccia, D. The size distribution of farms and international productivity differences. Am. Econ. Rev. 104, 1667–1697 (2014).
    Article  Google Scholar 

    24.
    Wang, J., Chen, K. Z., Gupta, S. D. & Huang, Z. Is small still beautiful? A comparative study of rice farm size and productivity in China and India. China Agr. Econ. Rev. 7, 484–509 (2015).
    Article  Google Scholar 

    25.
    Lu, H., Xie, H., He, Y., Wu, Z. & Zhang, X. Assessing the impacts of land fragmentation and plot size on yields and costs: a translog production model and cost function approach. Agr. Syst. 161, 81–88 (2018).
    Article  Google Scholar 

    26.
    Syp, A., Faber, A., Borzecka-Walker, M. & Osuch, D. Assessment of greenhouse gas emissions in winter wheat farms using data envelopment analysis approach. Pol. J. Environ. Stud. 24, 2197–2203 (2015).
    CAS  Article  Google Scholar 

    27.
    Li, G., Feng, Z., You, L. & Fan, L. Re-examining the inverse relationship between farm size and efficiency. China Agr. Econ. Rev. 5, 473–488 (2013).
    Article  Google Scholar 

    28.
    Fan, L. et al. Decreasing farm number benefits the mitigation of agricultural non-point source pollution in China. Environ. Sci. Pollut. Res. 26, 464–472 (2019).
    Article  Google Scholar 

    29.
    Cassman, K. G., Dobermann, A., Walters, D. T. & Yang, H. Meeting cereal demand while protecting natural resources and improving environmental quality. Annu. Rev. Env. Resour. 28, 315–358 (2003).
    Article  Google Scholar 

    30.
    Pellegrini, P. & Fernández, R. J. Crop intensification, land use, and on-farm energy-use efficiency during the worldwide spread of the green revolution. Proc. Natl Acad. Sci. USA 115, 2335–2340 (2018).
    CAS  Article  Google Scholar 

    31.
    Resource and Environment Data Cloud Platform (Resource and Environment Science and Data Center, 2018); http://www.resdc.cn/Default.aspx

    32.
    Laborde, D., Martin, W., Swinnen, J. & Vos, R. COVID-19 risks to global food security. Science 369, 500–502 (2020).
    ADS  CAS  Article  Google Scholar 

    33.
    Shi, Q., Jin, H. & Zhuo, J. Does land expropriation definitely reduce farmers’ income: a survey of 7 villages in Shanghai: the defects and reforms of the current land expropriation system [in Chinese]. Manage. World 3, 77–82 (2011).
    Google Scholar 

    34.
    Liu, Y. & Li, Y. Revitalize the world’s countryside. Nature 548, 275–277 (2017).
    ADS  CAS  Article  Google Scholar 

    35.
    Liu, Y., Fang, F. & Li, Y. Key issues of land use in China and implications for policy making. Land Use Policy 40, 6–12 (2014).
    CAS  Article  Google Scholar 

    36.
    Measures for Land Acquisition Compensation and Social Security for Land-Expropriated Farmers in Jiangsu Province Provincial Government Order No. 93 (Jiangsu Provincial People’s Government, 2013).

    37.
    Wu, Y., Chen, Y., Deng, X. & Hui, E. C. M. Development of characteristic towns in China. Habitat Int. 77, 21–31 (2018).
    Article  Google Scholar 

    38.
    Yu, Y., Huang, Y. & Zhang, W. Modeling soil organic carbon change in croplands of China, 1980–2009. Glob. Planet Change 82–83, 115–128 (2012).
    ADS  Article  Google Scholar 

    39.
    No. 1 Central Document (Ministry of Agriculture and Rural Affairs of the People’s Republic of China, 2020); http://www.moa.gov.cn/ztzl/jj2020zyyhwj/

    40.
    Güneralp, B. et al. Global scenarios of urban density and its impacts on building energy use through 2050. Proc. Natl Acad. Sci. USA 114, 8945–8950 (2017).
    Article  Google Scholar  More

  • in

    No projected global drylands expansion under greenhouse warming

    1.
    D’Odorico, P. & Porporato, A. Dryland Ecohydrology (Springer, 2019).
    2.
    Smith, W. K. et al. Remote sensing of dryland ecosystem structure and function: progress, challenges, and opportunities. Remote Sens. Environ. 233, 111401 (2019).
    Article  Google Scholar 

    3.
    Reynolds, J. F. et al. Global desertification: building a science for dryland development. Science 316, 847–851 (2007).
    CAS  Article  Google Scholar 

    4.
    Ahlström, A. et al. The dominant role of semi-arid ecosystems in the trend and variability of the land CO2 sink. Science 348, 895–899 (2015).
    Article  CAS  Google Scholar 

    5.
    Middleton, N. & Thomas, D. S. G. World Atlas of Desertification 2nd edn (Wiley, 1997).

    6.
    Budyko, M. I. & Miller, D. H. International Geophysics Series: Climate and Life Vol. 18 (Academic Press, 1974).

    7.
    Feng, S. & Fu, Q. Expansion of global drylands under a warming climate. Atmos. Chem. Phys. 13, 10081–10094 (2013).
    CAS  Article  Google Scholar 

    8.
    Fu, Q. & Feng, S. Responses of terrestrial aridity to global warming. J. Geophys. Res. Atmos. 119, 7863–7875 (2014).
    Article  Google Scholar 

    9.
    Scheff, J. & Frierson, D. M. W. Terrestrial aridity and its response to greenhouse warming across CMIP5 climate models. J. Clim. 28, 5583–5600 (2015).
    Article  Google Scholar 

    10.
    Huang, J., Yu, H., Guan, X., Wang, G. & Guo, R. Accelerated dryland expansion under climate change. Nat. Clim. Change 6, 166–171 (2016).
    Google Scholar 

    11.
    Huang, J., Yu, H., Dai, A., Wei, Y. & Kang, L. Drylands face potential threat under 2 °C global warming target. Nat. Clim. Change 7, 417–422 (2017).
    Article  Google Scholar 

    12.
    Park, C.-E. et al. Keeping global warming within 1.5 °C constrains emergence of aridification. Nat. Clim. Change 8, 70–74 (2018).
    Article  Google Scholar 

    13.
    Koutroulis, A. G. Dryland changes under different levels of global warming. Sci. Total Environ. 655, 482–511 (2019).
    CAS  Article  Google Scholar 

    14.
    Park, C. E. et al. Inequal responses of drylands to radiative forcing geoengineering methods. Geophys. Res. Lett. 46, 14011–14020 (2019).
    Article  Google Scholar 

    15.
    Wei, Y. et al. Drylands climate response to transient and stabilized 2 °C and 1.5 °C global warming targets. Clim. Dyn. 53, 2375–2389 (2019).
    Article  Google Scholar 

    16.
    Yao, J. et al. Accelerated dryland expansion regulates future variability in dryland gross primary production. Nat. Commun. 11, 1665 (2020).
    CAS  Article  Google Scholar 

    17.
    Berdugo, M. et al. Global ecosystem thresholds driven by aridity. Science 367, 787–790 (2020).
    CAS  Article  Google Scholar 

    18.
    Rajaud, A. & de Noblet-Ducoudré, N. Tropical semi-arid regions expanding over temperate latitudes under climate change. Climatic Change 144, 703–719 (2017).
    Article  Google Scholar 

    19.
    Yang, Y. et al. Disconnection between trends of atmospheric drying and continental runoff. Water Resour. Res. 54, 4700–4713 (2018).
    Article  Google Scholar 

    20.
    Greve, P., Roderick, M. L., Ukkola, A. M. & Wada, Y. The aridity index under global warming. Environ. Res. Lett. 14, 124006 (2019).
    CAS  Article  Google Scholar 

    21.
    Milly, P. C. D. & Dunne, K. A. Potential evapotranspiration and continental drying. Nat. Clim. Change 6, 946–949 (2016).
    Article  Google Scholar 

    22.
    Yang, Y., Roderick, M. L., Zhang, S., McVicar, T. R. & Donohue, R. J. Hydrologic implications of vegetation response to elevated CO2 in climate projections. Nat. Clim. Change 9, 44–48 (2019).
    Article  CAS  Google Scholar 

    23.
    Norby, R. J. & Zak, D. R. Ecological lessons from free-air CO2 enrichment (FACE) experiments. Annu. Rev. Ecol. Evol. Syst. 42, 181–203 (2011).
    Article  Google Scholar 

    24.
    Berg, A. & Sheffield, J. Soil moisture–evapotranspiration coupling in CMIP5 models: relationship with simulated climate and projections. J. Clim. 31, 4865–4878 (2018).
    Article  Google Scholar 

    25.
    Mahowald, N. et al. Projections of leaf area index in Earth system models. Earth Syst. Dyn. 7, 211–229 (2016).
    Article  Google Scholar 

    26.
    Sherwood, S. & Fu, Q. A drier future? Science 343, 737–739 (2014).
    CAS  Article  Google Scholar 

    27.
    Berg, A. et al. Land–atmosphere feedbacks amplify aridity increase over land under global warming. Nat. Clim. Change 6, 869–874 (2016).
    Article  Google Scholar 

    28.
    Berg, A. & Sheffield, J. Climate change and drought: the soil moisture perspective. Curr. Clim. Change Rep. 4, 180–191 (2018).
    Article  Google Scholar 

    29.
    Lavergne, A. et al. Observed and modelled historical trends in the water‐use efficiency of plants and ecosystems. Glob. Change Biol. 25, 2242–2257 (2019).
    Article  Google Scholar 

    30.
    Friedlingstein, P. Carbon cycle feedbacks and future climate change. Phil. Trans. R. Soc. A 373, 20140421 (2015).
    Article  CAS  Google Scholar 

    31.
    Swann, A. L., Hoffman, F. M., Koven, C. D. & Randerson, J. T. Plant responses to increasing CO2 reduce estimates of climate impacts on drought severity. Proc. Natl Acad. Sci. USA 113, 10019–10024 (2016).
    CAS  Article  Google Scholar 

    32.
    Lemordant, L., Gentine, P., Swann, A. S., Cook, B. I. & Scheff, J. Critical impact of vegetation physiology on the continental hydrologic cycle in response to increasing CO2. Proc. Natl Acad. Sci. USA 115, 4093–4098 (2018).
    CAS  Article  Google Scholar 

    33.
    Berg, A. & Sheffield, J. Evapotranspiration partitioning in CMIP5 models: uncertainties and future projections. J. Clim. 32, 2653–2671 (2019).
    Article  Google Scholar 

    34.
    Cao, L., Bala, G., Caldeira, K., Nemani, R. & Ban-Weiss, G. Importance of carbon dioxide physiological forcing to future climate change. Proc. Natl Acad. Sci. USA 107, 9513–9518 (2010).
    CAS  Article  Google Scholar 

    35.
    Skinner, C. B., Poulsen, C. J. & Mankin, J. S. Amplification of heat extremes by plant CO2 physiological forcing. Nat. Commun. 9, 1094 (2018).
    Article  CAS  Google Scholar 

    36.
    Kooperman, G. J. et al. Forest response to rising CO2 drives zonally asymmetric rainfall change over tropical land. Nat. Clim. Change 8, 434–440 (2018).
    Article  Google Scholar 

    37.
    Frieler, K. et al. Assessing the impacts of 1.5 °C global warming—simulation protocol of the Inter-sectoral Impact Model Intercomparison Project (ISIMIP2b). Geosci. Model Dev. 10, 4321–4345 (2017).
    Article  Google Scholar 

    38.
    Zhu, Z. et al. Greening of the Earth and its drivers. Nat. Clim. Change 6, 791–795 (2016).
    CAS  Article  Google Scholar 

    39.
    He, B., Wang, S., Guo, L. & Wu, X. Aridity change and its correlation with greening over drylands. Agric. For. Meteorol. 278, 107663 (2019).
    Article  Google Scholar 

    40.
    Brandt, M. et al. Human population growth offsets climate-driven increase in woody vegetation in sub-Saharan Africa. Nat. Ecol. Evol. 1, 0081 (2017).
    Article  Google Scholar 

    41.
    Burrell, A. L., Evans, J. P. & De Kauwe, M. G. Anthropogenic climate change has driven over 5 million km2 of drylands towards desertification. Nat. Commun. 11, 3853 (2020).
    CAS  Article  Google Scholar 

    42.
    Berg, A., Sheffield, J. & Milly, P. C. D. Divergent surface and total soil moisture projections under global warming. Geophys. Res. Lett. 44, 236–244 (2017).
    Article  Google Scholar 

    43.
    Mankin, J. S., Seager, R., Smerdon, J. E., Cook, B. I. & Williams, A. P. Mid-latitude freshwater availability reduced by projected vegetation responses to climate change. Nat. Geosci. 12, 983–988 (2019).
    CAS  Article  Google Scholar 

    44.
    Liu, Y. et al. Field-experiment constraints on the enhancement of the terrestrial carbon sink by CO2 fertilization. Nat. Geosci. 12, 809–814 (2019).
    CAS  Article  Google Scholar 

    45.
    Zeng, Z. et al. Responses of land evapotranspiration to Earth’s greening in CMIP5 Earth System Models. Environ. Res. Lett. 11, 104006 (2016).
    Article  Google Scholar 

    46.
    Peñuelas, J. et al. Shifting from a fertilization-dominated to a warming-dominated period. Nat. Ecol. Evol. 1, 1438–1445 (2017).
    Article  Google Scholar 

    47.
    Brodribb, T. J., Powers, J., Cochard, H. & Choat, B. Hanging by a thread? Forests and drought. Science 368, 261–266 (2020).
    CAS  Article  Google Scholar 

    48.
    Scheff, J., Seager, R., Liu, H. & Coats, S. Are glacials dry? Consequences for paleoclimatology and for greenhouse warming. J. Clim. 30, 6593–6609 (2017).
    Article  Google Scholar 

    49.
    Ault, T. R. On the essentials of drought in a changing climate. Science 368, 256–260 (2020).
    CAS  Article  Google Scholar 

    50.
    Berg, A. & Sheffield, J. Historic and projected changes in coupling between soil moisture and evapotranspiration (ET) confounded by the role of different ET components. J. Geophys. Res. Atmos. 124, 5791–5806 (2019).
    Google Scholar 

    51.
    Berg, A. & McColl, K. R code for ‘No global drylands expansion under greenhouse warming’. Zenodo https://doi.org/10.5281/zenodo.4490414 (2021). More

  • in

    Biodiversity’s importance is growing in China’s urban agenda

    Many cities in China, such as Xi’an (pictured), have experienced rapid growth in the past few decades.Credit: Xinhua/Shutterstock

    On 28 January 2020, a team of Chinese conservation scientists distributed a questionnaire across social-media platforms, asking Chinese citizens how they felt about proposed legislation that would ban the consumption and trade of wildlife in the country.
    It was an apposite moment: the questionnaire hit social-media platforms such as WeChat and Weibo just days after China had been forced to close its major cities to prevent the spread of a disease that scientists suspected was transferred to humans from an animal species at a market in Wuhan.
    More than 90% of the 74,070 respondents were in favour of a complete ban on wildlife trade — and, a month later, the central government came to the same conclusion and legislated to that effect. Researchers are increasingly studying the impact of these policies, and the country’s biodiversity. But big questions remain about whether China will deliver on its growing list of environmental commitments.

    Bin Zhao, an ecologist at Fudan University in Shanghai, China, says that, since the start of the COVID-19 pandemic, people in urban areas have been paying more attention to biodiversity than ever before. “People realized that contact with wild animals could lead to an outbreak of an epidemic, even in urban areas. This not only enhanced people’s understanding of biodiversity, but also promoted the idea that wildlife-protection law needed to be improved,” says Zhao.
    It came at a time when China was already committed to changing its approach to ecological protection, he says. In 2018, China amended its constitution to include the goal of becoming an ‘ecological civilization’. In the words of Chinese President Xi Jinping in 2017, economic development could no longer be at the expense of the environment.
    Multiple environmentally friendly policies have already been announced, such as the introduction of an ‘ecological red line’ policy to protect more of the Chinese mainland from development (see ‘Protected land’); a new network of national parks; stricter supervision of conservation; and a streamlining of environmental-oversight agencies — all to meet a government target of making the country’s environment ‘beautiful’ by 2035.

    Sources: UN/Xinhua/OECD

    Big cities, few controls
    In 1950, about only 13% of China’s population lived in cities. But since the 1980s, the country’s cities have grown rapidly as the engines of its economic growth (see ‘Urban population’). Millions left homes in rural areas to forge more prosperous lives in growing and newly built cities. Government policies, aimed at bolstering the economy, helped to encourage close to two-thirds of China’s population to move to these new urban areas, and the nation continues to have one of the world’s fastest growing urban populations. This has put intense pressure on the country’s ecology.

    Sources: UN/Xinhua/OECD

    “From an economic perspective, our ecosystems and environment have historically been considered to be worthless,” says Zhao. China’s natural resources, such as its wetlands, forests and water sources, haven’t received the same level of care from authorities as targets for economic growth, he says (see ‘Vegetation change’).

    Sources: UN/Xinhua/OECD

    As urban areas grow, there are direct and indirect impacts on ecological systems, according to Rob McDonald, who researches the impact and dependencies of cities on the natural world at The Nature Conservancy in Washington DC.
    Land is repurposed for development, and natural resources are needed to construct buildings and provide food and water for city dwellers, he says. These changes can lead to environmental problems, such as water and air pollution, insufficient water availability and deforestation much farther afield than in urban areas themselves.
    China’s government has been open about its commitment to tackling these problems, says Alice Hughes, a zoologist at the Xishuangbanna Tropical Botanical Garden in Menglun town, China. In May 2021, China will host the fifteenth United Nations Convention on Biological Diversity, also known as COP 15, in Kunming, where 200 countries will meet to sign off on a legally binding set of global targets to protect the world’s biodiversity. The country has already contributed to some broader environmental targets, including being carbon neutral by 2060.
    China has had some success, most notably in reducing air pollution. For example, in 2017, the amount of fine particulate matter in Beijing’s air dropped by just under 40% from the level in 2013, the year when national targets were launched.
    But at a press conference to discuss China’s progress on ecological and environmental protection, Cui Shuhong, an official at the Ministry of Ecology and Environment, said the country has much more to do to alleviate the fundamental pressures placed on its natural resources by economic development.
    Zhengguang Zhu, an environmental officer at China’s National Marine Environmental Monitoring Center, is familiar with preparations for COP 15: there are multiple working groups operating within the Ministry of Ecology and Environment, which are each responsible for different aspects of the event, from logistics to setting targets for improvements to China’s environment.

    Live turtles on display at a wildlife market in Shanghai, China, in August 2020. During the COVID-19 pandemic, the Chinese government issued a policy banning wildlife trade for food, but trade of exotic animals as pets still continues.Credit: Ales Plavevski/EPA-EFE/Shutterstock

    These working groups ask China’s public bodies, such as the ministry of agriculture, to offer their opinions on what the country feels should be included in the final roadmap for the coming decade.
    “I think the meeting will show that China has done its homework and is willing to be a good host. But leadership is not just about hospitality. It’s about having an ambitious framework that enables change, and I think we’ve got a long way to go before that happens,” says Zhu.
    Behaviour change
    Conservation researcher Tien Ming Lee, based at the Sun Yat-sen University in Guangzhou, China, says scientists and politicians are currently focused on finding better ways to protect Chinese ecosystems while continuing the country’s urban economic growth.
    His research team works across a range of projects, all focused on finding ways to prompt people to act differently and sustainably. For example, he is currently part of a 4-year, €10-million (US$12 million) project, mainly funded by the European Union, called Partners against Wildlife Crime. The project, which began in January 2019, hopes to disrupt the illicit supply chains through which exotic animals and plants, specifically tigers (Panthera tigris), Asian elephants (Elephas maximus), Siamese rosewood (Dalbergia cochinchinensis) and freshwater turtles, are traded throughout Cambodia, China, Laos, Malaysia, Myanmar, Thailand and Vietnam.
    As part of this project, Lee’s team and Lishu Li at the Wildlife Conservation Society China Counter Wildlife Trafficking Program are developing marketing materials to change the buying habits of urban Chinese consumers by attempting to dissuade them from illegal acts, such as buying tiger bone or elephant skin online for jewellery and traditional medicine, or keeping endangered freshwater turtles as pets. Lee says the materials have been developed with behavioural-science techniques: they aim to appeal to consumers’ desire to be seen to act in a conscientious manner.

    Police patrol the wetlands of the Yellow River Estuary ecotourism area near Dongying City, China.Credit: Costfoto/Barcroft Media via Getty

    Lee has also been part of a research project that looked at how trade agreements that stem from the country’s international Belt and Road economic initiative, an infrastructure project that aims to link trade across Europe, Asia and Africa to China, could lead to a greater demand for traditional Chinese medicine across the world. The plant, animal and fungal products used in these practises are often sourced from the wild, which might exacerbate the illegal and unsustainable trade of those species, he says.
    His research, a collaboration with Amy Hinsley, a conservation biologist at the University of Oxford, UK, concluded that there was a clear, urgent need for China to introduce carefully managed supply chains and ensure that rural farmers have resources for sustainable farming.
    During her four-decade career, Lu Zhi, a conservation biologist at Peking University in Beijing, has seen a shift in her field’s focus. It moved from observing animals in their natural habitats and coming up with ways to protect them from human activity to observing human behaviour: studying what can be done to make people’s lives more ecologically sustainable.
    In 2017, Zhi’s Shanshui Conservation Center, a non-governmental organization she founded in 2007 to develop community-based conservation projects, began working with herdsmen in Qinghai province on the Tibetan Plateau. The team wanted to help them to develop livelihoods from conservation activities in an underdeveloped, highly biodiverse area of China. The villagers learnt how to patrol and monitor wildlife, and how to act as guides for tourists interested in animal watching — including for the elusive and endangered snow leopard (Panthera uncia). Similar projects have been rolled out in 42 villages in western China.
    Zhi admits that such small projects are certainly not enough to bring the paradigm shift needed to safeguard the country’s vulnerable ecosystems. Government intervention has proved to be effective in tackling the larger issues, such as air and water pollution, she says. But “it’s not fair to ask people in rural areas not to develop their lives for the sake of wildlife, while others live in prosperous cities. We need alternative solutions.” More

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    Malaria trends in Ethiopian highlands track the 2000 ‘slowdown’ in global warming

    1.
    Pascual, M., Ahumada, J., Chaves, L. F., Rodó, X. & Bouma, M. Malaria resurgence in East African Highlands: temperature trends revisited. Proc. Natl Acad. Sci. USA 103, 5829–5834 (2006).
    ADS  CAS  PubMed  Article  Google Scholar 
    2.
    Alonso, D., Bouma, M. J. & Pascual, M. Epidemic malaria and warmer temperatures in recent decades in an East African highland. Proc. Roy. Soc. B Biol. Sci. 278, 1661–1669 (2011).
    Google Scholar 

    3.
    Stern, D. I. et al. Temperature and malaria trends in highland East Africa. PLoS ONE 6, e24524 (2011).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    4.
    Chaves, L. F. & Koenraadt, C. J. M. Climate change and highland malaria: fresh air for a hot debate. Quart. Rev. Biol. 85, 27–55 (2010).
    PubMed  Article  Google Scholar 

    5.
    Shanks, G. D., Hay, S. I., Omumbo, J. A. & Snow, R. W. Malaria in Kenya’s Western Highlands. Emerg. Infect. Dis. 11, 1425–1432 (2005).
    PubMed  PubMed Central  Article  Google Scholar 

    6.
    Omumbo, J. A., Lyon, B., Waweru, S. M., Connor, S. J. & Thomson, M. C. Raised temperatures over the Kericho tea estates: revisiting the climate in the East African highlands malaria debate. Mal. J. 10, 12 (2011).
    Article  Google Scholar 

    7.
    Siraj, A. S. et al. Altitudinal changes in malaria incidence in highlands of Ethiopia and Colombia. Science 343, 1154–1158 (2014).
    ADS  CAS  PubMed  Article  Google Scholar 

    8.
    Caminade, C. et al. Climate change and malaria: model intercomparison. Proc. Natl Acad. Sci. USA 111, 3286–3291 (2014).

    9.
    Mordecai, E. A. et al. Thermal biology of mosquito-borne disease. Ecol. Lett. 22, 1690–1708 (2019).
    PubMed  PubMed Central  Article  Google Scholar 

    10.
    Shapiro, L. L. M., Whitehead, S. A. & Thomas, M. B. Quantifying the effects of temperature on mosquito and parasite traits that determine the transmission potential of human malaria. PLoS Biol. 15, e2003489 (2017).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    11.
    Waite, J. L., Suh, E., Lynch, P. A., & Thomas, M. B. Exploring the lower thermal limits for development of the human malaria parasite, Plasmodium falciparum. Biol. Lett. 15, 20190275 (2019).

    12.
    Brohan, P., Kennedy, J. J., Harris, I., Tett, S. F. & Jones, P. D. Uncertainty estimates in regional and global observed temperature changes: a new dataset from 1850. J. Geophys. Res. Atmos. 111, D12106 (2006).
    ADS  Article  Google Scholar 

    13.
    Kerr, R. What happened to global warming? Scientists say just wait a bit. Science 326, 28–29 (2009).
    ADS  CAS  PubMed  Article  Google Scholar 

    14.
    Meehl, G. A., Arblaster, J. M., Fasullo, J. T., Hu, A. & Trenberth, K. E. Model-based evidence of deep-ocean heat uptake during surface-temperature hiatus periods. Nat. Clim. Change 1, 360–364 (2011).
    ADS  Article  Google Scholar 

    15.
    Stocker, T. F. et al (eds). Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change 153 (2013).

    16.
    Otto, O. et al. Energy budget constraints on climate response. Nat. Geosc. 6, 415–416 (2013).
    ADS  CAS  Article  Google Scholar 

    17.
    Fyfe, J. C., Gillett, N. P. & Zwiers, F. W. Overestimated global warming over the past 20 years. Nat. Clim. Change 3, 767–769 (2013).
    ADS  Article  Google Scholar 

    18.
    Kosaka, Y. & Xie, S.-P. Recent global-warming hiatus tied to equatorial Pacific surface cooling. Nature 501, 403–407 (2013).
    ADS  CAS  PubMed  Article  Google Scholar 

    19.
    Santer et al. Volcanic contribution to decadal changes in tropospheric temperature. Nat. Geosc. 7, 185–189 (2014).
    ADS  CAS  Article  Google Scholar 

    20.
    Trenberth, K. & Fasullo, J. An apparent hiatus in global warming? Earth’s Future 1, 19–32 (2013).
    ADS  Article  Google Scholar 

    21.
    Smith, D. Has global warming stalled? Nat. Clim. Change 3, 618–619 (2013).
    ADS  Article  Google Scholar 

    22.
    Guemas, V., Doblas-Reyes, F. J., Andreu-Burillo, I. & Asif, M. Retrospective prediction of the global warming slowdown in the past decade. Nat. Clim. Change 3, 649–653 (2013).
    ADS  Article  Google Scholar 

    23.
    Chen, X. & Tung, K.-K. Varying planetary heat sink led to global-warming slowdown and acceleration. Science 345, 897–903 (2014).
    ADS  CAS  PubMed  Article  Google Scholar 

    24.
    Boykoff, M. Media discourse on the climate slowdown. Nat. Clim. Change 4, 156–158 (2014).
    ADS  Article  Google Scholar 

    25.
    Hawkins, E., Edwards, T. & McNeall, D. Pause for thought. Nat. Clim. Change 4, 154–156 (2014).
    ADS  Article  Google Scholar 

    26.
    England, M. H. et al. Recent intensification of wind-driven circulation in the pacific and the ongoing warming hiatus. Nat. Clim. Change 4, 222–227 (2014).
    ADS  Article  Google Scholar 

    27.
    Karl, T. R. et al. Possible artifacts of data biases in the recent global surface warming hiatus. Science 348, 1469–1472 (2015).
    ADS  CAS  PubMed  Article  Google Scholar 

    28.
    Cowtan et al. Robust comparison of climate models with observations using blended land air and ocean sea surface temperatures. Geophys. Res. Lett. 42, https://doi.org/10.1002/2015GL064888 (2015).

    29.
    Cohen, J. L., Furtado, J. C., Barlow, M., Alexeev, V. A. & Cherry, J. E. Asymmetric seasonal temperature trends. Geophys. Res. Lett. 39, L22705 (2012).
    Google Scholar 

    30.
    Medhaug, I., Stolpe, M. B., Fischer, E. M. & Knutti, R. Reconciling controversies about the ‘global warming hiatus’. Nature 545, 41–47 (2017).
    ADS  CAS  PubMed  Article  Google Scholar 

    31.
    Balmaseda, M. A., Trenberth, K. E. & Källén, E. Distinctive climate signals in reanalysis of global ocean heat content. Geophys. Res. Lett. 40, 1754–175928 (2013).
    ADS  Article  Google Scholar 

    32.
    Wills, R. C., Schneider, T., Wallace, J. M., Battisti, D. S. & Hartmann, D. L. Disentangling global warming, multidecadal variability, and El Niño in Pacific temperatures. Geophys. Res. Lett. 45, 2487–249 (2018).
    ADS  Article  Google Scholar 

    33.
    Cai, W. et al. Pantropical climate interactions. Science 363, eaav4236 (2019).

    34.
    Aregawi, M. et al. Time series analysis of trends in malaria cases and deaths at hospitals and the effect of antimalarial interventions, 2001–2011, Ethiopia. PLoS ONE 9, e106359 (2014).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    35.
    Taffese, H. S. et al. Malaria epidemiology and interventions in Ethiopia from 2001 to 2016. Infect. Dis. Poverty 7, 103 (2018).
    PubMed  PubMed Central  Article  Google Scholar 

    36.
    Vautard, R., Yiou, P. & Ghil, M. Singular-spectrum analysis: a toolkit for short, noisy chaotic signals. Phys. D 58, 95–126 (1992).
    Article  Google Scholar 

    37.
    Ghil, M. et al. Advanced spectral methods for climatic time series. Rev. Geophys. 40, 1–41 (2002).
    Article  Google Scholar 

    38.
    Harris, T. J. & Yuan, H. Filtering and frequency interpretations of singular spectrum analysis. Phys. D 239, 1958–1967 (2010).
    MathSciNet  CAS  MATH  Article  Google Scholar 

    39.
    Anyamba, A., Tucker, C. J. & Eastman, J. R. NDVI anomaly patterns over Africa during the 1997/1998 ENSO warm event. Int. J. Rem. Sens. 22, 1847–1859 (2001).
    Article  Google Scholar 

    40.
    Nicholson, S. E. & Kim, J. The relationship of the El Niño Southern oscillation to African rainfall. Int. J. Climatol. 17, 117–135 (1997).
    Article  Google Scholar 

    41.
    Reason, C. J. C. & Rouault, M. ENSO-like decadal variability and South African rainfall. Geophys. Res. Lett. 29, 1638 (2002).
    ADS  Article  Google Scholar 

    42.
    Rodó, X. Reversal of three global atmospheric fields linking changes in SST anomalies in the Pacific, Atlantic and Indian ocean at tropical latitudes and midlatitudes. Clim. Dyn. 18, 203–217 (2001).
    Article  Google Scholar 

    43.
    Rodó, X., Pascual, M., Fuchs, G. & Faruque, A. S. G. ENSO and cholera: A nonstationary link related to climate change? Proc. Natl Acad. Sci. USA 99, 12901–12906 (2002).
    ADS  PubMed  Article  CAS  Google Scholar 

    44.
    Saji, N. et al. A dipole mode in the tropical Indian Ocean. Nature 401, 360–363 (1999).
    ADS  CAS  PubMed  Google Scholar 

    45.
    Neale, R. B. et al. Description of the NCAR Community Atmosphere Model (CAM 5.0), NCAR/TN-486+STR. http://www.cesm.ucar.edu/models/cesm1.0/cam/docs/description/cam5_desc.pdf (2012).

    46.
    Shanks, D., Hay, S., Stern, D., Biomndo, K. & Snow, R. Meteorologic Influences on Plasmodium falciparum malaria in the highland tea estates of Kericho, Western Kenya. Emerg. Infect. Dis. 12, 1404–1408 (2002).
    Article  Google Scholar 

    47.
    Negash, et al. Malaria Epidemics in the Highlands of Ethiopia. East Afr. Med. J. 82, https://doi.org/10.4314/eamj.v82i4.9279 (2005).

    48.
    Taffese, H. S. et al. Malaria epidemiology and interventions in Ethiopia from 2001 to 2016. Infect. Dis. Poverty 7, 103 (2018).

    49.
    Fetene, et al. The Ethiopian health extension program and variation in health systems performance: what matters? PLoS ONE 11, e0156438 (2016).

    50.
    PMI, Presidents Malaria Initiative. Ethiopia, Malaria Operational Plan FY, 2018. https://www.pmi.gov/docs/default-source/default-document-library/malaria-operational-plans/fy-2018/fy-2018-ethiopia-malaria-operational-plan.pdf?sfvrsn=5 (2018).

    51.
    Aregawi, et al. Time series analysis of trends in malaria cases and deaths at hospitals and the effect of antimalarial interventions, 2001–2011, Ethiopia. PLoS ONE 9, e106359 (2014).

    52.
    Roy, M., Bouma, M. J., Ionides, E. L., Dhiman, R. C. & Pascual, M. The potential elimination of Plasmodium vivax malaria by relapse treatment: insights from a transmission model and surveillance data from NW India. PLoS Negl. Trop. Dis. 7, 1–10 (2013).
    Article  Google Scholar 

    53.
    Rhein, M., Rintoul, S. R., & Aoki, S. in Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of The Intergovernmental Panel on Climate Change (2013).

    54.
    Roxy, M. K., Ritika, K., Terray, P. & Masson, S. The curious case of Indian Ocean Warming. J. Clim. 27, 8501–8509 (2014).
    ADS  Article  Google Scholar 

    55.
    Diro, G. T. DiroD., Grimes, I. F. & Black, E. Teleconnections between Ethiopian summer rainfall and sea surface temperature: Part I-observation and modelling. Clim. Dyn. 37, 103–119 (2010).
    Article  Google Scholar 

    56.
    Beltrando, G. & Camberlin, P. Interannual variability of rainfall in the eastern horn of Africa and indicators of atmospheric circulation. Int. J. Climatol. 13, 533–546 (1993).
    Article  Google Scholar 

    57.
    Gissila, T., Black, E., Grimes, E., & Slingo, J. M. Seasonal forecasting of the Ethiopian Summer rains. Int. J. Climatol. 24, https://doi.org/10.1002/joc.1078. (2004).

    58.
    Hansen, J., Sato, M., Kharecha, P. & von Schuckmann, K. Earth’s energy imbalance and implications. Atmos. Chem. Phys. 11, 13421–13449 (2011).
    ADS  CAS  Article  Google Scholar 

    59.
    Korecha, D. & Barnston, A. G. Predictability of June-September Rainfall in Ethiopia. Monthly Weather Rev. 135, 628–650 (2007).
    ADS  Article  Google Scholar 

    60.
    Funk, C. et al. Warming of the Indian Ocean threatens eastern and southern African food security but could be mitigated by agricultural development. Proc. Nat. Acad. Sci. USA 105, 11081–11086 (2008).
    ADS  CAS  PubMed  Article  Google Scholar 

    61.
    Williams, A. P. & Funk, C. A. Westward extension of the warm pool leads to a westward extension of the Walker circulation, drying eastern Africa. Clim. Dyn. 37, 2417–2435 (2011).
    Article  Google Scholar 

    62.
    Hoell, A., Hoerling, M., Eischeid, Quan, X., & Liebmann, B. Reconciling Theories for Human and Natural Attribution of Recent East Africa Drying. J. Clim. 30, https://doi.org/10.1175/JCLI-D-16-0558.1. (2016).

    63.
    Kucharski, F., Kang, I. S., Farneti, R. & Feudale, L. Tropical Pacific response to 20th century Atlantic warming. Geophys. Res. Lett. 38, L03702 (2011).
    ADS  Article  Google Scholar 

    64.
    Kug, J.-S. & Kang, I.-S. Interactive feedback between ENSO and the Indian Ocean. J. Clim. 19, 1784–1801 (2006).
    ADS  Article  Google Scholar 

    65.
    Luo, J.-J., Sasaki, W. & Masumoto, Y. Indian Ocean warming modulates Pacific climate change. Proc. Natl Acad. Sci. USA 109, 18 701–18 706 (2012).
    CAS  Article  Google Scholar 

    66.
    Meyrowitsch, D. W. et al. Is the current decline in malaria burden in sub-Saharan Africa due to a decrease in vector population? Malar. J. 10, 188 (2011).
    PubMed  PubMed Central  Article  Google Scholar 

    67.
    Baeza, A., Bouma, M. J., Dhiman, R. & Pascual., M. Malaria control under unstable dynamics: reactive vs. climate-based strategies. Acta Trop. Spec. Sect. Hum. Infect. Dis. Environ. Chang. 129, 42–51 (2014).
    Google Scholar 

    68.
    Harris, I., Jones, P. D., Osborn, T. J. & Lister, D. H. Updated high-resolution grids of monthly climatic observations – the CRU TS3.10 Dataset. Int. J. Climatol. 34, 623–642 (2014).
    Article  Google Scholar 

    69.
    Kalnay, E. et al. The NCEP/NCAR 40-year reanalysis project. Bull. Am. Met. Soc. 77, 437–471 (1996).
    ADS  Article  Google Scholar 

    70.
    Rayner, N. A. et al. Global analyses of sea surface temperature, sea ice, and night marine air temperature since the late nineteenth century. J. Geophys. Res. 108, 4407 (2003).
    Article  Google Scholar 

    71.
    Mantua, N. J., Hare, S. R., Zhang, Y., Wallace, J. M. & R., C. Francis A Pacific interdecadal climate oscillation with impacts on salmon production. Bull. Am. Met. Soc. 78, 1069–1079 (1997).
    ADS  Article  Google Scholar 

    72.
    Thomson, D. J. Spectrum estimation and harmonic analysis. Proc. IEEE 70, 1055–1096 (1982).
    ADS  Article  Google Scholar 

    73.
    Percival, D. B., and Walden, A. T. Spectral Analysis for Physical Applications: Multitaper and Conventional Univariate Techniques (1993).

    74.
    Press, W. H., Teukolsky, S. A., Vetterling, W. T. & Flannery, B. P. Section 13.4.3. Multitaper Methods and Slepian Functions, Numerical Recipes: The Art of Scientific Computing 3rd edn. (2007).

    75.
    Rodríguez-Arias, M. A. & Rodó, X. A primer on the study of transitory dynamics in ecological series using the scale-dependent correlation analysis. Oecologia 138, 485–504 (2004).
    ADS  PubMed  Article  Google Scholar 

    76.
    Rodó, X. & Rodríguez-Arias, M. A. A new method to detect transitory signatures and local time/space variability structures in the climate system: the scale-dependent correlation analysis. Clim. Dyn. 27, 441–458 (2006).
    Article  Google Scholar 

    77.
    Laneri, K. et al. Forcing versus feedback: epidemic malaria and monsoon rains in northwest India. PLoS Comput. Biol. 6, e1000898 (2010).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    78.
    Laneri, K. et al. Dynamical malaria models reveal how immunity buffers effect of climate variability. Proc. Nat. Acad. Sci. USA 112, 8786–8791 (2015).
    ADS  CAS  PubMed  Article  Google Scholar 

    79.
    Roy, M., Bouma, M., Dhiman, R. C. & Pascual, M. Predictability of epidemic malaria under non-stationary conditions with process-based models combining epidemiological updates and climate variability. Malar. J. 14, 1 (2015).
    Article  CAS  Google Scholar 

    80.
    Ionides, E., Bretó, C. & King, A. Inference for nonlinear dynamical systems. Proc. Natl Acad. Sci. USA 103, 18438–18443 (2006).
    ADS  CAS  PubMed  Article  Google Scholar 

    81.
    King, A., Nguyen, D. & Ionides, E. Statistical inference for partially observed Markov processes via the R package pomp. J. Stat. Softw. 69, 1–43 (2016).
    Article  Google Scholar 

    82.
    Hurrell, J. W., Hack, J., Shea, D., Caron, J. & Rosinski, J. A new sea surface temperature and sea ice boundary dataset for the community atmosphere model. J. Clim. 21, 5145–5153 (2008).
    ADS  Article  Google Scholar 

    83.
    Meinshausen, M. et al. The RCP greenhouse gas concentrations and their extension from 1765 to 2300. Clim. Change https://doi.org/10.1007/s10584-011-0156-z (2011).

    84.
    Cionni et al. Ozone database in support of CMIP5 simulations: results and corresponding radiative forcing. Atmos. Chem. Phys. 11, 11267–11292 (2011).
    ADS  CAS  Article  Google Scholar 

    85.
    Lamarque et al. CAM-chem: description and evaluation of interactive atmospheric chemistry in the Community Earth System Model. Geophys. Mod. Dev. 5, 369–411 (2012).
    Article  Google Scholar 

    86.
    Danielson, J. J. & Gesch, D. B. Global multi-resolution terrain elevation data 2010 (GMTED2010). Open-file report 2011-1073 (2011). More