Ecology

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

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

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

1.
Naeem, S., Duffy, J. E. & Zavaleta, E. The functions of biological diversity in an age of extinction. Science 336, 1401–1406 (2012).
ADS  CAS  PubMed  Article  Google Scholar 
2.
Curtis, P. G., Slay, C. M., Harris, N. L., Tyukavina, A. & Hansen, M. C. Classifying drivers of global forest loss. Science 361, 1108–1111 (2018).
ADS  CAS  PubMed  Article  Google Scholar 

3.
Ewers, R. M. & Didham, R. K. Confounding factors in the detection of species responses to habitat fragmentation. Biol. Rev. 81, 117–142 (2006).
PubMed  Article  Google Scholar 

4.
Jones, G., Jacobs, D. S., Kunz, T. H., Willig, M. R. & Racey, P. A. Carpe noctem: the importance of bats as bioindicators. Endanger. Species Res. 8, 93–115 (2009).
Article  Google Scholar 

5.
Rocha, R. et al. Design matters: an evaluation of the impact of small man-made forest clearings on tropical bats using a before-after-control-impact design. For. Ecol. Manag. 401, 8–16 (2017).
Article  Google Scholar 

6.
Wood, J. R. et al. No single driver of biodiversity: divergent responses of multiple taxa across land use types. Ecosphere 8, e01997 (2017).
Article  Google Scholar 

7.
Coutinho Cunto, G. C. & Bernard, E. Neotropical bats as indicators of environmental disturbance: what is the emerging message?. Acta Chiropterologica 14, 143–151 (2012).
Article  Google Scholar 

8.
Medellín, R. A., Equihua, M. & Amin, M. A. Bat diversity and abundance as indicators of disturbance in neotropical rainforest. Conserv. Biol. 14, 1666–1675 (2000).
Article  Google Scholar 

9.
Russo, D., Bosso, L. & Ancillotto, L. Novel perspectives on bat insectivory highlight the value of this ecosystem service in farmland: research frontiers and management implications. Agric. Ecosyst. Environ. 266, 31–38 (2018).
Article  Google Scholar 

10.
Avila-Cabadilla, L. D., Stoner, K. E., Henry, M. & Alvarez Añorve, M. Y. Composition, structure and diversity of phyllostomid bat assemblages in different successional stages of a tropical dry forest. For. Ecol. Manag. 258, 986–996 (2009).
Article  Google Scholar 

11.
Castro-Luna, A. A., Sosa, V. J. & Castillo-Campos, G. Quantifying phyllostomid bats at different taxonomic levels as ecological indicators in a disturbed tropical forest. Acta Chiropterologica 9, 219–228 (2007).
Article  Google Scholar 

12.
García-Morales, R., Badano, E. I. & Moreno, C. E. Response of neotropical bat assemblages to human land use. Conserv. Biol. 27, 1096–1106 (2013).
PubMed  Article  Google Scholar 

13.
Meyer, C. F. J. & Kalko, E. K. V. Bat assemblages on neotropical land-bridge islands: nested subsets and null model analyses of species co-occurrence patterns. Divers. Distrib. 14, 644–654 (2008).
Article  Google Scholar 

14.
Farneda, F. Z. et al. Predicting biodiversity loss in island and countryside ecosystems through the lens of taxonomic and functional biogeography. Ecography 43, 97–106 (2020).
Article  Google Scholar 

15.
Cisneros, L. M., Fagan, M. E. & Willig, M. R. Season-specific and guild-specific effects of anthropogenic landscape modification on metacommunity structure of tropical bats. J. Anim. Ecol. 84, 373–385 (2015).
PubMed  Article  Google Scholar 

16.
Peña-Cuellar, E., Stoner, K. E., Avila-Cabadilla, L. D., Martínez-Ramos, M. & Estrada, A. Phyllostomid bat assemblages in different successional stages of tropical rain forest in Chiapas, Mexico. Biodivers. Conserv. 21, 1381–1397 (2012).
Article  Google Scholar 

17.
Fenton, A. M. B. et al. Phyllostomid bats (Chiroptera: Phyllostomidae) as indicators of habitat disruption in the Neotropics. Biotropica 24, 440–446 (1992).
Article  Google Scholar 

18.
Avila-Cabadilla, L. D. et al. Local and landscape factors determining occurrence of phyllostomid bats in tropical secondary forests. PLoS ONE 7, e35228 (2012).
ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

19.
Falcão, L. A. D., do Espírito-Santo, M. M., Fernandes, G. W. & Paglia, A. P. Effects of habitat structure, plant cover, and successional stage on the bat assemblage of a tropical dry forest at different spatial scales. Diversity 10, 1–11 (2018).
Article  Google Scholar 

20.
Avila-Cabadilla, L. D. et al. Phyllostomid bat occurrence in successional stages of neotropical dry forests. PLoS ONE 9, e84572 (2014).
ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

21.
Falcão, L. A. D., do Espírito-Santo, M. M., Leite, L. O., Garro, R. N. S. L., Avila-Cabadilla, L. D. & Stoner, K. E. Spatiotemporal variation in phyllostomid bat assemblages over a successional gradient in a tropical dry forest in southeastern Brazil. J. Trop. Ecol. 30, 123–132 (2014).
Article  Google Scholar 

22.
Zarazúa-Carbajal, M., Avila-Cabadilla, L. D., Alvarez-Añorve, M. Y., Benítez-Malvido, J. & Stoner, K. E. Importance of riparian habitat for frugivorous bats in a tropical dry forest in western Mexico. J. Trop. Ecol. 33, 74–82 (2017).
Article  Google Scholar 

23.
Meyer, C. F. J., Struebig, M. J. & Willig, M. R. Responses of tropical bats to habitat fragmentation, logging, and deforestation. In Bats in the Anthropocene: conservation of bats in a changing world (eds. Voigt, C. C. & Kingston, T.) 63–103 (Springer International Publishing) doi:https://doi.org/10.1007/978-3-319-25220-9 (2016).

24.
Estrada, A. & Coates-Estrada, R. Bats in continuous forest, forest fragments and in an agricultural mosaic habitat-island at Los Tuxtlas, Mexico. Biol. Conserv. 103, 237–245 (2002).
Article  Google Scholar 

25.
Galindo-González, J. Clasificación de los murciélagos de la región de Los Tuxtlas, Veracruz, respecto a su respuesta a la fragmentación del hábitat. Acta Zoológica Mex. 20, 239–243 (2004).
Google Scholar 

26.
Gorrensen, M. & Willing, M. R. Landscape responses of bats to habitat fragmentation in Atlantic forest of Paraguay. J. Mammal. 85, 688–697 (2004).
Article  Google Scholar 

27.
de Oliveira, H. F. M., de Camargo, N. F., Gager, Y. & Aguiar, L. M. S. The response of bats (Mammalia: Chiroptera) to habitat modification in a neotropical savannah. Trop. Conserv. Sci. 10, 1–14 (2017).
Article  Google Scholar 

28.
de la Peña-Cuéllar, E., Benítez-Malvido, J., Avila-Cabadilla, L. D., Martínez-Ramos, M. & Estrada, A. Structure and diversity of phyllostomid bat assemblages on riparian corridors in a human-dominated tropical landscape. Ecol. Evol. 5, 903–913 (2015).
PubMed  PubMed Central  Article  Google Scholar 

29.
García-Morales, R. et al. Deforestation impacts on bat functional diversity in tropical landscapes. PLoS ONE 11, 1–16 (2016).
Article  CAS  Google Scholar 

30.
Daniel, S., Korine, C. & Pinshow, B. Central-place foraging in nursing, arthropod-gleaning bats. Can. J. Zool. 86, 623–626 (2008).
Article  Google Scholar 

31.
Galindo-González, J. & Sosa, V. J. Frugivorous bats in isolated trees and riparian vegetation associated with human-made pastures in a fragmented tropical landscape. Southwest. Nat. 48, 579–589 (2003).
Article  Google Scholar 

32.
Chazdon, R. L. et al. Rates of change in tree communities of secondary neotropical forests following major disturbances. Philos. Trans. R. Soc. B Biol. Sci. 362, 273–289 (2007).
Article  Google Scholar 

33.
Brito, J., Camacho, M. A., Romero, V. & Vallejo, A. F. Mamíferos del Ecuador. Versión 2019.0. Museo de Zoología, Pontificia Universidad Católica del Ecuador. https://bioweb.bio/faunaweb/mammaliaweb (2019).

34.
Tirira, D. A field guide to the mammals of Ecuador. Asociación Ecuatoriana de Mastozoología and Murciélago Blanco Publishing House (2017).

35.
Jara-Guerrero, A., Maldonado Riofrío, D., Espinosa, C. I. & Duncan, D. H. Beyond the blame game: a restoration pathway reconciles ecologists’ and local leaders’ divergent models of seasonally dry tropical forest degradation. Ecol. Soc. 24, 22 (2019).
Article  Google Scholar 

36.
Cueva Ortiz, J. et al. Influence of anthropogenic factors on the diversity and structure of a dry forest in the central part of the Tumbesian region (Ecuador-Perú). Forests 10, 1–22 (2019).
Article  Google Scholar 

37.
Medina, A., Harvey, C. A., Sánchez Merlo, D., Vílchez, S. & Hernández, B. Bat diversity and movement in an agricultural landscape in Matiguás, Nicaragua. Biotropica 39, 120–128 (2007).
Article  Google Scholar 

38.
Davies, K. F., Margules, C. R. & Lawrence, J. F. Which traits of species predict population declines in experimental forest fragments?. Ecology 81, 1450–1461 (2000).
Article  Google Scholar 

39.
Henle, K., Davies, K. F., Kleyer, M., Margules, C. & Settele, J. Predictors of species sensitivity to fragmentation. Biodivers. Conserv. 13, 207–251 (2004).
Article  Google Scholar 

40.
Medellin, R. A. Chrotopterus auritus. Mamm. Species 343, 1–5 (1989).
Google Scholar 

41.
Aguirre, L. F., Lens, L., Van Damme, R. & Matthysen, E. Consistency and variation in the bat assemblages inhabiting two forest islands within a neotropical savanna in Bolivia. J. Trop. Ecol. 19, 367–374 (2003).
Article  Google Scholar 

42.
Stoner, K. E. Phyllostomid bat community structure and abundance in two contrasting tropical dry forests. Biotropica 37, 591–599 (2005).
Article  Google Scholar 

43.
Gotelli, N. J. & Colwell, R. K. Estimating species richness. In Biological diversity: frontiers in measurement and assessment (eds. Magurran, A. & McGill, B. J.) 39–54 (Oxford University Press, 2011).

44.
Moreno, C. E. & Halffter, G. Assessing the completeness of bat biodiversity inventories using species accumulation curves. J. Appl. Ecol. 37, 149–158 (2000).
Article  Google Scholar 

45.
Colwell, R. K. & Coddington, J. A. Estimating terrestrial biodiversity through extrapolation. Philos. Trans. Biol. Sci. 345, 101–118 (1994).
ADS  CAS  Article  Google Scholar 

46.
Baselga, A. Partitioning the turnover and nestedness components of beta diversity. Glob. Ecol. Biogeogr. 19, 134–143 (2010).
Article  Google Scholar 

47.
Baselga, A. Separating the two components of abundance-based dissimilarity: balanced changes in abundance vs. abundance gradients. Methods Ecol. Evol. 4, 552–557 (2013).
Article  Google Scholar 

48.
Mena, J. L. & Williams de Castro, M. Diversidad y patrones reproductivos de quirópteros en un área urbana de Lima, Perú. Ecol. Apl. 1, 1–8 (2002).
Article  Google Scholar 

49.
Pacheco, V., Cadenillas, R., Salas, E., Tello, C. & Zeballos, H. Diversidad y endemismo de los mamíferos del Perú. Rev. Peru. Biol. 16, 5–32 (2009).
Google Scholar 

50.
Pinto, C. M., Marchán-Rivadeneira, M. R., Tapia, E. E., Carrera, J. P. & Baker, R. J. Distribution, abundance and roosts of the fruit bat Artibeus fraterculus (Chiroptera: Phyllostomidae). Acta Chiropterologica 15, 85–94 (2013).
Article  Google Scholar 

51.
Homyack, J. A. Evaluating habitat quality of vertebrates using conservation physiology tools. Wildl. Res. 37, 332–342 (2010).
Article  Google Scholar 

52.
Carrasco-Rueda, F. & Loiselle, B. A. Do riparian forest strips in modified forest landscapes aid in conserving bat diversity?. Ecol. Evol. 9, 4192–4209 (2019).
PubMed  PubMed Central  Article  Google Scholar 

53.
Lewis, S. E. Roost fidelity of bats: a review. Am. Soc. Mammal. Roost 76, 481–496 (1995).
Google Scholar 

54.
Voss, R. S., Fleck, D. W., Strauss, R. E., Velazco, P. M. & Simmons, N. B. Roosting ecology of Amazonian bats: evidence for guild structure in hyperdiverse mammalian communities. Am. Museum Novit. 3870, 1–43 (2016).
Article  Google Scholar 

55.
Hylander, K. & Ehrle, J. The mechanisms causing extinction debts. Trends Ecol. Evol. 28, 341–346 (2013).
PubMed  Article  Google Scholar 

56.
Willig, M. R. et al. Guild-level responses of bats to habitat conversion in a lowland Amazonian rainforest: species composition and biodiversity. J. Mammal. 100, 223–238 (2019).
PubMed  PubMed Central  Article  Google Scholar 

57.
Meyer, C. F. J. Methodological challenges in monitoring bat population- and assemblage-level changes for anthropogenic impact assessment. Mamm. Biol. 80, 159–169 (2015).
Article  Google Scholar 

58.
Gibb, R., Browning, E., Glover-Kapfer, P. & Jones, K. E. Emerging opportunities and challenges for passive acoustics in ecological assessment and monitoring. Methods Ecol. Evol. 10, 169–185 (2019).
Article  Google Scholar 

59.
Sikes, R. S. & the Animal Care and Use Committee of the American Society of Mammalogists. 2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. J. Mammal. 97, 663–688 (2016).

60.
Espinosa, C. I. et al. Bosques tropicales secos de la región Pacífico Ecuatorial: diversidad, estructura, funcionamiento e implicaciones para la conservación. Ecosistemas 21, 167–179 (2012).
Google Scholar 

61.
García-Cervigón, A. I., Camarero, J. J. & Espinosa, C. I. Intra-annual stem increment patterns and climatic responses in five tree species from an Ecuadorian tropical dry forest. Trees 31, 1057–1067 (2017).
Article  Google Scholar 

62.
Jara-Guerrero, A., De la Cruz, M. & Méndez, M. Seed dispersal spectrum of woody species in South Ecuadorian dry forests: environmental correlates and the effect of considering species abundance. Biotropica 43, 722–730 (2011).
Article  Google Scholar 

63.
Vázquez, M., Larrea, M. & Ojeda, P. Biodiversidad en los bosques secos del suroccidente de la provincia de Loja (EcoCiencia, 2001).
Google Scholar 

64.
Tapia-Armijos, M. F., Homeier, J., Espinosa, C. I., Leuschner, C. & De La Cruz, M. Deforestation and forest fragmentation in south Ecuador since the 1970s-losing a hotspot of biodiversity. PLoS ONE 10, e133701 (2015).
Google Scholar 

65.
Cueva Ortiz, J. & Chalán, L. A. Cobertura vegetal y uso actual del suelo de la provincia de Loja. Informe Técnico (2010).

66.
Kalka, M. & Kalko, E. K. V. Gleaning bats as underestimated predators of herbivorous insects: diet of Micronycteris microtis (Phyllostomidae) in Panama. J. Trop. Ecol. 22, 1–10 (2006).
Article  Google Scholar 

67.
Espinosa, C. I., Valle, D., Armijos, D., Jara-Guerrero, A. & Griffith, D. M. Bat abundance data from Zapotillo, Ecuador 2013–2017. Knowl. Netw. Biocomplexity https://doi.org/10.5063/F1765CQJ (2020).
Article  Google Scholar 

68.
Barwell, L. J., Isaac, N. J. B. & Kunin, W. E. Measuring β-diversity with species abundance data. J. Anim. Ecol. 84, 1112–1122 (2015).
PubMed  PubMed Central  Article  Google Scholar 

69.
Jakob, E. M., Marshall, S. D. & Uetz, G. W. Estimating fitness: a comparison of body condition indices. Oikos 77, 61–67 (1996).
Article  Google Scholar 

70.
Reist, J. D. An empirical evaluation of several univariate methods that adjust for size variation in morphometric data. Can. J. Zool. 63, 1429–1439 (1985).
ADS  Article  Google Scholar 

71.
Oksanen, J. et al. vegan: Community Ecology Package. R package version 2.5-6. https://CRAN.R-project.org/package=vegan (2019).

72.
R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/ (2018). More

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

An improved reference genome of P. alba var. pyramidalis
To identify the major structural variation between the genomes of these two species, we first produced a chromosome-level genome assembly of P. alba var. pyramidalis using single-molecule sequencing and chromosome conformation capture (Hi-C) technologies, and then performed comparative genomic analysis with a recently published genome assembly of P. euphratica37. The resulting assembly of P. alba var. pyramidalis consisted of 131 contigs spanning 408.08 Mb, 94.74% (386.61 Mb) of which were anchored onto 19 chromosomes (Supplementary Fig. S1 and Supplementary Tables S1–S3). A total of 40,215 protein-coding genes were identified in this assembly (Supplementary Table S4). The content of repetitive elements in the genome of P. alba var. pyramidalis (138.17 Mb, 33.86% of the genome) is 188.94 Mb less than that of P. euphratica (327.11 Mb, 56.95% of the genome), which contributes greatly to their differences in genome size (Supplementary Table S5).
3D organization of the poplar genomes
To characterize the spatial organization and evolution of poplar 3D genomes at a high resolution, we performed Hi-C experiments using HindIII for P. euphratica and P. alba var. pyramidalis, generating a total of 482.95 million sequencing read pairs. These data were mapped to their respective reference genome sequences. After stringent filtering, 81.72 and 94.61 million usable valid read pairs were obtained in P. euphratica and P. alba var. pyramidalis, respectively, and used for subsequent comparative 3D genome analysis (Supplementary Table S6). In addition, we profiled the DNA methylation and transcriptomes of the same tissue samples to provide a framework for understanding the relationships among epigenetic features and 3D chromatin architecture in poplar.
We first examined genome packing at the chromosomal level with a genome-wide Hi-C map at 50 kb binning resolution for P. euphratica and P. alba var. pyramidalis. As expected, the normalized Hi-C map from both species showed intense signals on the main diagonal (Fig. 1, and Supplementary Figs. S2 and S3) and a rapid decrease in the frequency of intrachromosomal interactions with increasing genomic distance, indicating frequent interactions between sequences close to each other in the linear genome (Supplementary Fig. S4). Strong intrachromosomal and interchromosomal interactions were also observed on the chromosome arms, implying the presence of chromosome territories in the nucleus, in which each chromosome occupies a limited, exclusive nuclear space16,38.
Fig. 1: Hi-C heatmaps with compartment region analysis results at 50-kb resolution of P. euphratica chromosome 1 (left) and P. alba var. pyramidalis chromosome 1 (right).

The heatmaps at the top are Hi-C contact maps at 50-kb resolution, which show global patterns of chromatin interaction in the chromosome. The chromosome is shown from top to bottom and left to right. The ICE-normalized interaction intensity is shown on the color scale on the right side of the heatmap. The track below the Hi-C heatmap shows the partition of A (red histogram, PC1  > 0) and B (green histogram, PC1 5 kb) structural variants ranging from 5 to 446 kb in length in the alignment of the two genomes, including 719 inversions, 476 translocations, and 7947 and 10,093 unique regions in P. alba var. pyramidalis and P. euphratica, respectively (Supplementary Tables S10 and S11).
To characterize the relationship between structural variation and spatial organization of the poplar genomes, we first analyzed the conservation of A/B compartments between P. alba var. pyramidalis and P. euphratica, using a 50-kb Hi-C matrix. The results showed that 71.52% (145.75 Mb in P. euphratica and 145.63 Mb in P. alba var. pyramidalis) of the total length of the syntenic regions have the same compartment status between the two species, while 43.68 and 43.71 Mb of the genomic regions exhibit A/B compartment switching in P. alba var. pyramidalis and P. euphratica, respectively (Fig. 3a). For the regions with structural variation, we found that 77% of the inversion events between the two genomes had no effects on their compartment status, while 61% of the translocation events occurred within the regions exhibiting compartment switching (Fig. 4a and Supplementary Table S10). Moreover, we also found that 38.59% and 33.39% of the nonsyntenic regions were identified as A compartments in P. alba var. pyramidalis and P. euphratica, respectively, indicating that the large-scale insertions and/or deletions are biased to occur at heterochromatic regions (Fig. 4b). We further assessed the conservation of genome organization at the TAD level by examining whether the orthologous genes within the same TAD in one species could still be located within the TAD in another species19,21,23. The results indicated that only 48.04% of TADs from P. alba var. pyramidalis and 40.95% from P. euphratica were substantially shared between the two species (Figs. 3b, c). Taken together, these results indicated that the 3D genome organization shows surprisingly low conservation across poplar species at both the compartmental and TAD levels.
Fig. 3: Evolutionary conservation of compartment status and TADs across P. euphratica and P. alba var. pyramidalis.

a Overlap of compartment status between syntenic regions in P. euphratica and P. alba var. pyramidalis. b Overlap of TADs between syntenic regions in P. euphratica and P. alba var. pyramidalis. c Example of conserved TAD structures across a syntenic region between P. euphratica and P. alba var. pyramidalis. The TADs are outlined by black triangles in the heatmaps, and the position of the TAD domains is indicated by alternating blue-green line segments. The mean cf value used to identify the domains is also shown. The orthology tracks of these conserved domains are shown at the bottom

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Fig. 4: Relationship between structural variation and spatial organization of the genomes of P. euphratica and P. alba var. pyramidalis.

a Analysis of compartment inversion (left) and translocation (right) across P. euphratica and P. alba var. pyramidalis. b Analysis of compartments of species-specific regions in P. euphratica (left) and P. alba var. pyramidalis (right)

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Relationship between chromatin interactions and expression divergence of WGD-derived paralogs
Poplar species have undergone a recent WGD event followed by diploidization, a process of genome fractionation that leads to functional and expression divergence of the duplicated gene pairs27,28,33. Although no biased gene loss or expression dominance was found between the two poplar subgenomes, there is evidence that nearly half of the WGD-derived paralogs have diverged in expression32,33. To explore the potential role of chromatin dynamics on the observed expression patterns of duplicated genes, we examined their differences in chromatin interaction patterns for both species. We first identified a total of 10,438 and 9754 paralogous gene pairs showing interchromosomal interactions in P. euphratica and P. alba var. pyramidalis, respectively. After correlating the frequency of chromatin interactions with their differences in expression, we found that gene pairs with biased expression (more than twofold differences in expression levels) interacted less frequently than gene pairs with similar expression levels in both species (P = 1.71 × 10−6 and 7.20 × 10−7 for P. euphratica and P. alba var. pyramidalis, respectively, Mann–Whitney U test; Fig. 5a). We also estimated the interaction score (the average of the distance-normalized interaction frequencies) for bins involved in the paralogous gene pairs and quantified their differences in interaction strength (Supplementary Fig. S7 and Supplementary Table S12)3,23. Our results showed that for gene pairs with biased expression, highly expressed gene copies have stronger interaction strengths than weakly expressed copies (P = 2.10 × 10−12 and 2.74 × 10−2 for P. alba var. pyramidalis and P. euphratica, respectively, Mann–Whitney U test), while no significant differences were observed for gene pairs with similar expression levels (Fig. 5b). We further investigated these phenomena at the level of high-order chromatin architecture and found that the gene pairs located in conserved TADs had similar expression levels (P = 2.68 × 10−3 and 7.86 × 10−6 for P. euphratica and P. alba var. pyramidalis, respectively, Mann–Whitney U test; Supplementary Fig. S8). Overall, our analyses indicate that the extensive expression divergence between WGD-derived paralogs in Populus is associated with the differences in their chromatin dynamics and 3D genome organization, and suggest that this organization may function as a key regulatory layer underlying expression divergence during diploidization.
Fig. 5: Comparison of interaction levels between WGD-derived paralogs with biased/similar expression in P. euphratica and P. alba var. pyramidalis.

a The box plot shows that the interaction frequency of WGD-derived paralogs with biased (fold change  > 2) and similar (fold change  More

Zoologist Alice Hughes leads the landscape-ecology research group at Xishuangbanna Tropical Botanical Garden in Menglun, Yunnan province, China.Credit: Michael C. Orr

British zoologist Alice Hughes has been working at the Xishuangbanna Tropical Botanical Garden in Menglun, Yunnan province, in southern China, for nearly eight years. She reveals what she has learnt about the country’s approach to ecological conservation ahead of its first United Nations biodiversity conference in Kunming, Yunnan, in May.
What is your current role?
I lead the landscape-ecology research group at one of China’s most diverse botanical gardens. My team aims to better understand the lives of animals and how they interact with their environments. This helps us to create more effective methods of conserving a biodiverse environment.
The 18-person team, which is part of the Chinese Academy of Sciences (CAS), does everything from mapping biodiversity to researching the illegal and legal trade in different species, to find out where and why our natural world is changing. We then develop actionable measures to help stem the worst effects of those changes.
For example, many members of my team are working on the various species of Rhinolophus bats. Our genetic research suggests that around 70% of the Rhinolophus bat species haven’t been described in scientific literature. If you can’t describe a species, then you can’t conserve it.
How did you come to work in China, and what’s it like?
In 2011, I moved to Thailand from the United Kingdom as part of my postdoctoral research, before heading to Australia and finally taking a position in China in 2013.
At first, I was naive about how different the culture might be in Asian countries and it’s definitely been a steep learning curve. Adaptability is important. I think that many people in the West are much too ready to disbelieve or find fault with actions from China, and Chinese scientists. As a result, there is sensitivity in China’s research community, especially around things that have frequently been an issue, such as the regulation of the trade of exotic wildlife. As a foreigner, it is a challenging balance to provide advice without it being seen as overly critical. I can participate in these discussions at a high level because I have worked here long enough: people know I will listen and provide my perspectives based on fact, rather than prejudice.

I’ve worked on some difficult and potentially sensitive topics, such as endangered species, wildlife trade and the Belt and Road Initiative, which aims to link global trade routes to China through international infrastructure development, for example. I focus on the possible impacts these might have on biodiversity and how to minimize them. China is wary of being accused of driving extensive biodiversity loss, especially as it is investing in scientific research to avert it.
I’ve been invited to join a variety of both central and regional government working groups. It’s a privilege to be in those groups and work with some of the country’s top scientists, especially when it comes to international or UN meetings.
Working for CAS is the equivalent to being an employee of the government. Many people outside China still find it surprising that foreigners work in scientific institutes here, even though the number is growing.
I’m also unusual because I’m a foreign woman. In the time I have worked here I don’t think I have met any other European women with full-time faculty positions in China. In my institute there are more than ten foreign men with such positions. It’s not easy for Chinese women either. At the institute, we have 43 research groups; only 3 are led by women.
It’s important for all conservation scientists to be open minded and willing to find out what’s going to work in any country and culture to help tackle the global problem of biodiversity loss, and develop solutions that work in that societal context. A good example of that came last year, when some specialists called for a global ban on wild-meat consumption, amid fears over new diseases that originate in wild animals and cause outbreaks in humans. Now that might sound like a great idea, but in many parts of Africa there is not enough water to raise livestock, and people depend on wild meat for food.
This means that rather than recommending a blanket ban, a better solution might be a system that monitors what is traded, and provides recommendations as to which species can be eaten safely and sustainably.

Xishuanganna tropical botanic garden in southwest China’s Yunnan Province.Credit: Xinhua/eyevine

Do foreign scientists need to speak Chinese to work in China?
For most of my team, neither English nor Chinese is their first language. We have around 12 different nationalities, so discussions take place predominantly in English, as a default.
I work closely with my Chinese colleagues to make sure that our research work is properly communicated when it’s published in Chinese. In meetings with Chinese colleagues, someone will translate pertinent points to me, or I’ll translate my slides into Chinese and present in English. I also have my reports and briefs translated, and with advances in translation software, we can get what is needed done.
It’s easy to have misunderstandings when you’re translating ideas between different languages, so we’re careful to look for any linguistic nuances that might change the perceived meaning.
How is China balancing urbanization with conservation?
It’s an ongoing challenge. The concept of an ecological civilization — the government’s vision for environmentally sustainable growth in China — was written into the country’s constitution in 2018 after it was made a national priority in 2012, which is a huge commitment to sustainability.
A principal policy is the ecological conservation red-line plan, an idea that has been developed over the past decade. Across China, large areas of land are now being protected from industrial and urban development, in part to ensure that crucial ecosystems, such as wetlands that limit floods, can continue to function effectively. Multimillion-dollar developments have been torn down during its roll-out. China is one of few countries to have enacted such a science-based, top-down vision of how to balance human need with the maintenance of ecological services and preservation of biodiversity.

It’s not all perfect, though: I know that on paper, these ecological red lines now exist and in certain biodiversity hotspots they have been enforced. But not every region is the same. Areas have high levels of autonomy and in Yunnan, where I live, there have been more challenges for the local government to work with provincial governments for many practical and political reasons. The saying goes, ‘The mountains are high, and the emperor is far away’: places that are far away from Beijing feel less pressure to enact centralized policies because there is less supervision.
The south of China has seen lots of deforestation, which is hugely damaging to biodiversity. Natural forests have been replaced with for-profit tree plantations, usually planted with rubber or eucalyptus, which have had a hugely negative impact on biodiversity. Sustainable forestry is a real issue across Asia.
China is leading an important biodiversity conference in May. What are your expectations?
It’s the first time that China will host the UN biodiversity conference and this puts the spotlight on what they are doing to help the situation.
I know there are a number of senior Chinese officials who would like to see China take on more of an international leadership role, in addition to making efforts to preserve biodiversity domestically.
The current set of UN goals for global biodiversity expired last year and the next set, which is planned to be agreed at the convention, must encourage countries to plant diverse, native species. Currently, there is no pressure coming from politicians to do that, even though we know we suffer biodiversity loss as a result: we’re often hung up on targets, even if those targets are virtue signalling, rather than real change.
Also, governments tend to try to meet their targets in the easiest and most economically beneficial way. So they meet their tree-planting targets by planting by just a few, non-diverse species that are often not even native to the country.
We still need to include more practical goals in policy documents, such as enabling sustainable supply chains, to focus on the mechanisms behind biodiversity loss.
What strikes you as unique about the Chinese ecological-research environment?
A Chinese ecologist needs to be fast to act. The time frame to submit an application for a grant can be very quick. Often you have less than 24 hours to respond. Also, most initiatives are tied to the government’s five-year plans, so our priorities need to adapt to reflect those five-year cycles.
In the past two years, there has been a complete inventory of all China’s marine and terrestrial protected areas so they can be accurately mapped and future targets can be based on them. That really is an unparalleled effort.
This involved mapping 400 marine protected areas, and 13,600 terrestrial ones. I haven’t heard of anything equivalent to this scale and speed in any other country.
The most positive thing for me is that science matters here. The annual budget for scientific research is increasing and the findings from our applied research inform national policy. That is something the West would do well to remember. More

1.
Ni, X. & Groffman, P. M. Declines in methane uptake in forest soils. Proc. Natl. Acad. Sci. USA 115, 8587–8590 (2018).
CAS  PubMed  Article  Google Scholar 
2.
IPCC. Climate change 2013: the physical science basis Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (Cambridge University Press, 2013).

3.
Kirschke, S. et al. Three decades of global methane sources and sinks. Nat. Geosci. 6, 813–823 (2013).
ADS  CAS  Article  Google Scholar 

4.
Turner, A. J., Frankenberg, C. & Kort, E. A. Interpreting contemporary trends in atmospheric methane. Proc. Natl. Acad. Sci. USA 116, 2805–2813 (2019).
CAS  PubMed  Article  Google Scholar 

5.
Tate, K. R. Soil methane oxidation and land-use change–from process to mitigation. Soil Biol. Biochem. 80, 260–272 (2015).
CAS  Article  Google Scholar 

6.
Thauer, R. K., Anne-Kristin, K., Henning, S., Wolfgang, B. & Reiner, H. Methanogenic archaea: ecologically relevant differences in energy conservation. Nat. Rev. Microbiol. 6, 579–591 (2008).
CAS  PubMed  Article  Google Scholar 

7.
Banger, K., Tian, H. & Lu, C. Do nitrogen fertilizers stimulate or inhibit methane emissions from rice fields?. Glob. Change Biol. 18, 3259–3267 (2012).
ADS  Article  Google Scholar 

8.
Murase, J. & Kimura, M. Methane production and its fate in paddy fields. IV. Sources of microorganisms and substrates responsible for anaerobic CH4 oxidation in subsoil. Soil Sci. Plant Nutr. 40, 57–61 (1994).
CAS  Article  Google Scholar 

9.
Zhang, M., Huang, J., Sun, S., Rehman, M. & He, S. Depth-specific distribution and significance of nitrite-dependent anaerobic methane oxidation process in tidal flow constructed wetlands used for treating river water. Sci. Total Environ. 716, 107354 (2020).
Google Scholar 

10.
Yu, X. et al. Sonneratia apetala introduction alters methane cycling microbial communities and increases methane emissions in mangrove ecosystems. Soil Biol. Biochem. 144, 107775 (2020).
CAS  Article  Google Scholar 

11.
Hanson, R. S. & Hanson, T. E. Methanotrophic bacteria. Microbiol. Rev. 60, 439–471 (1996).
CAS  PubMed  PubMed Central  Article  Google Scholar 

12.
Knief, C. Diversity and habitat preferences of cultivated and uncultivated aerobic methanotrophic bacteria evaluated based on pmoA as molecular marker. Front. Microbiol. 6, 1346 (2015).
PubMed  PubMed Central  Article  Google Scholar 

13.
Dunfield, P., Knowles, R., Dumont, R. & Moore, T. R. Methane production and consumption in temperate and subarctic peat soils: response to temperature and pH. Soil Biol. Biochem. 25, 321–326 (1993).
CAS  Article  Google Scholar 

14.
Mer, J. L. & Roger, P. Production, oxidation, emission and consumption of methane by soils: a review. Eur. J. Soil Biol. 37, 25–50 (2001).
Article  Google Scholar 

15.
Aronson, E. L., Dubinsky, E. A. & Helliker, B. R. Effects of nitrogen addition on soil microbial diversity and methane cycling capacity depend on drainage conditions in a pine forest soil. Soil Biol. Biochem. 62, 119–128 (2013).
CAS  Article  Google Scholar 

16.
Bodelier, P. L. E. & Laanbroek, H. J. Nitrogen as a regulatory factor of methane oxidation in soils and sediments. FEMS Microbiol. Ecol. 47, 265–277 (2004).
CAS  PubMed  Article  Google Scholar 

17.
Galloway, J. N. et al. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320, 889–892 (2008).
ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

18.
Liu, L. & Greaver, T. L. A review of nitrogen enrichment effects on three biogenic GHGs: the CO2 sink may be largely offset by stimulated N2O and CH4 emission. Ecol. Lett. 12, 1103–1117 (2009).
CAS  PubMed  Article  Google Scholar 

19.
Fowler, D., Coyle, M., Skiba, U., Sutton, M. A. & Voss, M. The global nitrogen cycle in the twenty-first century. Philos. Trans. R. Soc. B. 368, 20130164 (2013).
Article  CAS  Google Scholar 

20.
Reay, D. S., Dentener, F., Smith, P., Grace, J. & Feely, R. A. Global nitrogen deposition and carbon sinks. Nat. Geosci. 1, 430–437 (2008).
ADS  CAS  Article  Google Scholar 

21.
Ackerman, D., Millet, D. B. & Chen, X. Global estimates of inorganic nitrogen deposition across four decades. Glob. Biogeochem. Cycles 33, 100–107 (2019).
ADS  CAS  Article  Google Scholar 

22.
Liu, X. et al. Enhanced nitrogen deposition over China. Nature 494, 459–462 (2013).
ADS  CAS  PubMed  Article  Google Scholar 

23.
Li, Q. et al. Nitrogen depositions increase soil respiration and decrease temperature sensitivity in a Moso bamboo forest. Agric. For. Meteorol. 268, 48–54 (2019).
ADS  Article  Google Scholar 

24.
Steudler, P. A., Bowden, R. D., Melillo, J. M. & Aber, J. D. Influence of nitrogen fertilization on methane uptake in temperate forest soils. Nature 341, 314–316 (1989).
ADS  Article  Google Scholar 

25.
Hütsch, B. W., Webster, C. P. & Powlson, D. S. Methane oxidation in soil as affected by land use, soil pH and N fertilization. Soil Biol. Biochem. 26, 1613–1622 (1994).
Article  Google Scholar 

26.
Bodelier, P. L. E., Roslev, P., Henckel, T. & Frenzel, P. Stimulation by ammonium-based fertilizers of methane oxidation in soil around rice roots. Nature 403, 421–424 (2000).
ADS  CAS  PubMed  Article  Google Scholar 

27.
Kruger, M. & Frenzel, P. Effects of N-fertilisation on CH4 oxidation and production, and consequences for CH4 emissions from microcosms and rice fields. Glob. Change Biol. 9, 773–784 (2003).
ADS  Article  Google Scholar 

28.
Delgado, J. A. & Mosier, A. R. Mitigation alternatives to decrease nitrous oxides emissions and urea-nitrogen loss and their effect on methane flux. J. Environ. Qual. 25, 1105–1111 (1996).
CAS  Article  Google Scholar 

29.
Shang, Q. et al. Net annual global warming potential and greenhouse gas intensity in Chinese double rice-cropping systems: a 3-year field measurement in long-term fertilizer experiments. Glob. Change Biol. 17, 2196–2210 (2011).
ADS  Article  Google Scholar 

30.
Cai, Z. et al. Methane and nitrous oxide emissions from rice paddy fields as affected by nitrogen fertilizers and water management. Plant Soil 196, 7–14 (1997).
CAS  Article  Google Scholar 

31.
Malghani, S., Reim, A., Fischer, J. V., Conrad, R. & Trumbore, S. E. Soil methanotroph abundance and community composition are not influenced by substrate availability in laboratory incubations. Soil Biol. Biochem. 101, 184–194 (2016).
CAS  Article  Google Scholar 

32.
Schnyder, E., Bodelier, P. L. E., Hartmann, M., Henneberger, R. & Niklaus, P. A. Positive diversity-functioning relationships in model communities of methanotrophic bacteria. Ecology 99, 714–723 (2018).
PubMed  Article  Google Scholar 

33.
Wang, C., Liu, D. & Bai, E. Decreasing soil microbial diversity is associated with decreasing microbial biomass under nitrogen addition. Soil Biol. Biochem. 120, 126–133 (2018).
CAS  Article  Google Scholar 

34.
Shrestha, M., Shrestha, P. M., Frenzel, P. & Conrad, R. Effect of nitrogen fertilization on methane oxidation, abundance, community structure, and gene expression of methanotrophs in the rice rhizosphere. ISME J. 4, 1545–1556 (2010).
CAS  PubMed  Article  Google Scholar 

35.
Liu, H. et al. Responses of soil methanogens, methanotrophs, and methane fluxes to land-use conversion and fertilization in a hilly red soil region of southern China. Environ. Sci. Pollut. Res. 24, 8731–8743 (2017).
CAS  Article  Google Scholar 

36.
Bao, Q., Ding, L. J., Huang, Y. & Xiao, K. Effect of rice straw and/or nitrogen fertiliser inputs on methanogenic archaeal and denitrifying communities in a typical rice paddy soil. Earth Environ. Sci. Trans. R. Soc. Edinb. 109, 375–386 (2019).
CAS  Google Scholar 

37.
Ho, A. et al. The more, the merrier: heterotroph richness stimulates methanotrophic activity. ISME J. 8, 1945–1948 (2014).
PubMed  PubMed Central  Article  Google Scholar 

38.
Dan, H. et al. The response of methanotrophs to additions of either ammonium, nitrate or urea in alpine swamp meadow soil as revealed by stable isotope probing. FEMS Microbiol. Ecol. 7, fiz077 (2019).
Google Scholar 

39.
Zhang, D., Mo, L., Chen, X., Zhang, L. & Xu, X. Effect of nitrogen addition on methanotrophs in temperate forest soil. Acta Ecol. Sin. 37, 8254–8263 (2017).
Google Scholar 

40.
Mohanty, S. R., Bodelier, P. L. E., Floris, V. & Conrad, R. Differential effects of nitrogenous fertilizers on methane-consuming microbes in rice field and forest soils. Appl. Environ. Microbiol. 72, 1346–1354 (2006).
CAS  PubMed  PubMed Central  Article  Google Scholar 

41.
Hu, A. & Lu, Y. The differential effects of ammonium and nitrate on methanotrophs in rice field soil. Soil Biol. Biochem. 85, 31–38 (2015).
CAS  Article  Google Scholar 

42.
Shrestha, P. M. et al. Linking activity, composition and seasonal dynamics of atmospheric methane oxidizers in a meadow soil. ISME J. 6, 1115–1126 (2012).
CAS  PubMed  Article  Google Scholar 

43.
Jang, I., Lee, S., Zoh, K. D. & Kang, H. Methane concentrations and methanotrophic community structure influence the response of soil methane oxidation to nitrogen content in a temperate forest. Soil Biol. Biochem. 43, 620–627 (2011).
CAS  Article  Google Scholar 

44.
Song, X., Chen, X., Zhou, G., Jiang, H. & Peng, C. Observed high and persistent carbon uptake by Moso bamboo forests and its response to environmental drivers. Agric. For. Meteorol. 247, 467–475 (2017).
ADS  Article  Google Scholar 

45.
Song, X. et al. Carbon sequestration by Chinese bamboo forests, and their ecological benefits: assessment of potential, problems, and future challenges. Environ. Rev. 19, 418–428 (2011).
CAS  Article  Google Scholar 

46.
Jia, Y. et al. Spatial and decadal variations in inorganic nitrogen wet deposition in China induced by human activity. Sci. Rep. 4, 3763 (2014).
PubMed  PubMed Central  Article  CAS  Google Scholar 

47.
Song, X., Zhou, G., Gu, H. & Qi, L. Management practices amplify the effects of N deposition on leaf litter decomposition of the Moso bamboo forest. Plant Soil 395, 391–400 (2015).
CAS  Article  Google Scholar 

48.
Mo, J., Fang, Y., Xu, G., Li, D. & Xue, J. The short-term responses of soil CO2 emission and CH4 uptake to simulated N deposition in nursery and forests of Dinghushan in subtropical China. Acta Ecol. Sin. 25, 682–690 (2005).
CAS  Google Scholar 

49.
Zhang, W. et al. Methane uptake responses to nitrogen deposition in three tropical forests in southern China. J. Geophys. Res. 113, D11116 (2008).
ADS  Article  CAS  Google Scholar 

50.
Song, X. et al. Nitrogen addition increased CO2 uptake more than non-CO2 greenhouse gases emissions in a Moso bamboo forest. Sci. Adv. 6, eaaw5790 (2020).
ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

51.
Knief, C., Lipski, A. & Dunfield, P. F. Diversity and activity of methanotrophic bacteria in different upland soils. Appl. Environ. Microbiol. 69, 6703–6714 (2003).
CAS  PubMed  PubMed Central  Article  Google Scholar 

52.
Wang, M., Xu, X., Wang, W., Wang, G. & Su, C. Effects of slag and biochar amendments on methanogenic community structures in paddy fields. Acta Ecol. Sin. 38, 2816–2818 (2018).
Article  Google Scholar 

53.
Zeikus, J. G. Biology of methanogenic bacteria. Bacteriol. Rev. 41, 514–541 (1977).
CAS  PubMed  PubMed Central  Article  Google Scholar 

54.
Täumer, J. et al. Divergent drivers of the microbial methane sink in temperate forest and grassland soils. Glob. Change Biol. 27, 929–940 (2021).

55.
Pratscher, J., Vollmers, J., Wiegand, S., Dumont, M. G. & Kaster, A. K. Unravelling the identity, metabolic potential and global biogeography of the atmospheric methane-oxidizing upland soil cluster α. Environ. Microbiol. 20(3), 1016–1029 (2018).
CAS  PubMed  PubMed Central  Article  Google Scholar 

56.
Knief, C. Diversity and habitat preferences of cultivated and uncultivated aerobic methanotrophic bacteria evaluated based on pmoA as molecular marker. Front. Microbiol. 6, 487 (2015).
Article  Google Scholar 

57.
Deng, Y. et al. Upland soil cluster gamma dominates methanotrophic communities in upland grassland soils. Sci. Total Environ. 670, 826–836 (2019).
ADS  CAS  PubMed  Article  Google Scholar 

58.
Henckel, T., Friedrich, M. & Conrad, R. Molecular analyses of the methane-oxidizing microbial community in rice field soil by targeting the genes of the 16S rRNA, particulate methane monooxygenase, and methanol dehydrogenase. Appl. Environ. Microbiol. 65, 1980–1990 (1999).
CAS  PubMed  PubMed Central  Article  Google Scholar 

59.
Lieberman, R. L. & Rosenzweig, A. C. Biological methane oxidation: regulation, biochemistry, and active site structure of particulate methane monooxygenase. Crit. Rev. Biochem. Mol. Biol. 39, 147–164 (2004).
CAS  PubMed  Article  Google Scholar 

60.
Freitag, T. E. & Prosser, J. I. Correlation of methane production and functional gene transcriptional activity in a peat soil. Appl. Environ. Microbiol. 75, 6679–6687 (2009).
CAS  PubMed  PubMed Central  Article  Google Scholar 

61.
Thauer, R. K. Biochemistry of methanogenesis: a tribute to Marjory Stephenson: 1998 Marjory Stephenson prize lecture. Microbiology 144, 2377–2406 (1998).
CAS  PubMed  Article  Google Scholar 

62.
Schnell, S. & King, G. M. Mechanistic analysis of ammonium inhibition of atmospheric methane consumption in forest soils. Appl. Environ. Microbiol. 60, 3514–3521 (1994).
CAS  PubMed  PubMed Central  Article  Google Scholar 

63.
Chao, A. Nonparametric estimation of the number of classes in a population. Scand. J. Stat. 11, 265–270 (1984).
MathSciNet  Google Scholar 

64.
Shannon, C. E. A. mathematical theory of communication. Bell Syst. Tech. J. 27, 379–423 (1948).
MathSciNet  MATH  Article  Google Scholar 

65.
Li, Q. et al. Biochar amendment decreases soil microbial biomass and increases bacterial diversity in Moso bamboo (Phyllostachys edulis) plantations under simulated nitrogen deposition. Environ. Res. Lett. 13, 044029 (2018).
ADS  Article  CAS  Google Scholar 

66.
Li, Q., Song, X., Gu, H. & Gao, F. Nitrogen deposition and management practices increase soil microbial biomass carbon but decrease diversity in Moso bamboo plantations. Sci. Rep. 6, 28235 (2016).
ADS  PubMed  PubMed Central  Article  Google Scholar 

67.
Frey, S. D., Knorr, M., Parrent, J. L. & Simpson, R. T. Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. For. Ecol. Manag. 196, 159–171 (2004).
Article  Google Scholar 

68.
Lin, Y. et al. Long-term application of lime or pig manure rather than plant residues suppressed diazotroph abundance and diversity and altered community structure in an acidic ultisol. Soil Biol. Biochem. 123, 218–228 (2018).
CAS  Article  Google Scholar 

69.
Rousk, J. et al. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J. 4, 1340–1351 (2010).
PubMed  Article  Google Scholar 

70.
Zhou, X., Guo, Z., Chen, C. & Jia, Z. Soil microbial community structure and diversity are largely influenced by soil pH and nutrient quality in 78-year-old tree plantations. Biogeosciences 14, 2101–2111 (2017).
ADS  CAS  Article  Google Scholar 

71.
Nicol, G. W., Leininger, S., Schleper, C. & Prosser, J. I. The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ. Microbiol. 10, 2966–2978 (2008).
CAS  PubMed  Article  Google Scholar 

72.
Vitousek, P. M. et al. Technical report: human alteration of the global nitrogen cycle: sources and consequences. Ecol. Appl. 7, 737 (1997).
Google Scholar 

73.
Treseder, K. K. Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol. Lett. 11, 1111–1120 (2008).
PubMed  Article  Google Scholar 

74.
Serna-Chavez, H. M. & Bodegom, P. M. V. Global drivers and patterns of microbial abundance in soil. Glob. Ecol. Biogeogr. 22, 1162–1172 (2013).
Article  Google Scholar 

75.
Rosso, L., Lobry, J. R., Bajard, S. & Flandrois, J. P. Convenient model to describe the combined effects of temperature and pH on microbial growth. Appl. Environ. Microbiol. 61, 610–616 (1995).
CAS  PubMed  PubMed Central  Article  Google Scholar 

76.
Högberg, M. N., Högberg, P. & Myrold, D. D. Is microbial community composition in boreal forest soils determined by pH, C-to-N ratio, the trees, or all three?. Oecologia 150, 590–601 (2007).
ADS  PubMed  Article  Google Scholar 

77.
Sterner, R. W. & Elser, J. J. Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere (Princeton University Press, Princeton, 2002).
Google Scholar 

78.
Kolb, S. The quest for atmospheric methane oxidizers in forest soils. Environ. Microbiol. Rep. 1, 336–346 (2009).
CAS  PubMed  Article  Google Scholar 

79.
Topp, E. & Pettey, E. Soils as sources and sinks for atmospheric methane. Can. J. Soil Sci. 77, 167–177 (1997).
CAS  Article  Google Scholar 

80.
Bender, M. & Conrad, R. Effect of CH4 concentrations and soil conditions on the induction of CH4 oxidation activity. Soil Biol. Biochem. 27, 1517–1527 (1995).
CAS  Article  Google Scholar 

81.
Kolb, S., Knief, C., Dunfield, P. F. & Conrad, R. Abundance and activity of uncultured methanotrophic bacteria involved in the consumption of atmospheric methane in two forest soils. Environ. Microbiol. 7(8), 1150–1161 (2005).
CAS  PubMed  Article  Google Scholar 

82.
Degelmann, D. M., Borken, W., Drake, H. L. & Kolb, S. Different atmospheric methane-oxidizing communities in European Beech and Norway Spruce Soils. Appl. Environ. Microbiol. 76(10), 3228–3235 (2010).
CAS  PubMed  PubMed Central  Article  Google Scholar 

83.
Li, S., Yu, Y. & He, S. Summary of research on dissolved organic carbon (DOC). Soil Environ. Sci. 11, 422–429 (2002).
Google Scholar 

84.
Zhang, R. et al. Nitrogen deposition enhances photosynthesis in Moso bamboo but increases susceptibility to other stress factors. Front. Plant Sci. 8, 1975 (2017).
PubMed  PubMed Central  Article  Google Scholar 

85.
Wan, X. et al. Soil C:N ratio is the major determinant of soil microbial community structure in subtropical coniferous and broadleaf forest plantations. Plant Soil 387, 103–116 (2015).
CAS  Article  Google Scholar 

86.
Demoling, F., Figueroa, D. & Bååth, E. Comparison of factors limiting bacterial growth in different soils. Soil Biol. Biochem. 39, 485–2495 (2007).
Article  CAS  Google Scholar 

87.
Aronson, E. L. & Helliker, B. R. Methane flux in non-wetland soils in response to nitrogen addition: a meta-analysis. Ecology 91, 3242–3251 (2010).
CAS  Article  Google Scholar 

88.
Cheng, S. et al. The primary factors controlling methane uptake from forest soils and their responses to increased atmospheric nitrogen deposition: a review. Acta Ecol. Sin. 32, 4914–4923 (2012).
ADS  CAS  Article  Google Scholar 

89.
Fierer, N. et al. Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J. 6, 1007–1017 (2012).
CAS  PubMed  Article  Google Scholar 

90.
Ramirez, K. S., Craine, J. M. & Fierer, N. Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes. Glob. Change Biol. 18, 1918–1927 (2012).
ADS  Article  Google Scholar 

91.
Song, X., Li, Q. & Gu, H. Effect of nitrogen deposition and management practices on fine root decomposition in Moso bamboo plantations. Plant Soil 410, 207–215 (2017).
CAS  Article  Google Scholar 

92.
Vance, E. D., Brookes, P. C. & Jenkinson, D. S. An extraction method for measuring soil microbial biomass C. Soil Biol. Biochem. 19, 703–707 (1987).
CAS  Article  Google Scholar 

93.
Li, Y. et al. Biochar reduces soil heterotrophic respiration in a subtropical plantation through increasing soil organic carbon recalcitrancy and decreasing carbon-degrading microbial activity. Soil Biol. Biochem. 122, 173–185 (2018).
CAS  Article  Google Scholar 

94.
Lu, R. Methods for Soil Agro-chemistry Analysis (China Agricultural Science and Technology Press, Beijing, 2000).
Google Scholar 

95.
Bourne, D. G., Mcdonald, I. R. & Murrell, J. C. Comparison of pmoA PCR primer sets as tools for investigating methanotroph diversity in three Danish soils. Appl. Environ. Microbiol. 67, 3802 (2001).
CAS  PubMed  PubMed Central  Article  Google Scholar 

96.
Angel, R., Claus, P. & Conrad, R. Methanogenic archaea are globally ubiquitous in aerated soils and become active under wet anoxic conditions. ISME J. 6, 847–862 (2011).
PubMed  PubMed Central  Article  CAS  Google Scholar 

97.
Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336 (2010).
CAS  PubMed  PubMed Central  Article  Google Scholar 

98.
Wang, Q. et al. Ecological patterns of nifH genes in four terrestrial climatic zones explored with targeted metagenomics using FrameBot, a new informatics tool. mBio 4, e00592-e613 (2013).
PubMed  PubMed Central  Google Scholar 

99.
Kou, Y. et al. Scale-dependent key drivers controlling methane oxidation potential in Chinese grassland soils. Soil Biol. Biochem. 111, 104–114 (2017).
CAS  Article  Google Scholar 

100.
Kou, Y. et al. Climate and soil parameters are more important than denitrifier abundances in controlling potential denitrification rates in Chinese grassland soils. Sci. Total Environ. 669, 62–69 (2019).
ADS  CAS  PubMed  Article  Google Scholar 

101.
Wei, H. et al. Contrasting soil bacterial community, diversity, and function in two forests in China. Front. Microbiol. 9, 1693 (2018).
PubMed  PubMed Central  Article  Google Scholar 

102.
Liu, W. et al. Critical transition of soil bacterial diversity and composition triggered by nitrogen enrichment. Ecology 101, e03053 (2020).
PubMed  Google Scholar 

103.
Tang, X., Liu, S., Zhou, G., Zhang, D. & Zhou, C. Soil-atmospheric exchange of CO2, CH4, and N2O in three subtropical forest ecosystems in southern China. Glob. Change Biol. 12, 546–560 (2006).
ADS  Article  Google Scholar  More