Ecology

Biodiversity assessment through DNA metabarcodingOur analysis detected 160 Operational Taxonomic Units (OTUs) with 12,007,712 sequenced reads, 222,370 ± 41,954 (sd) reads per sample, for a total of 54 sequenced samples. The rarefaction curves showed good sequencing effort for the samples (Supplementary Figure S1) which were rarefied to the least count among samples corresponding to 135,443 reads. Twenty OTUs, (7.2% of the total), were assigned to taxa not relevant to our work (mainly to mosses and ferns during the periods October 2014–March 2015 and July–October 2015). From the remaining OTUs, 108 (88% of the reads) were taxonomically assigned to 32 families of vascular plants (68 identified taxa) (Table 2, Supplementary Table S1) and 32 OTUs (4.8% of the reads) remained unidentified either because of low sequence identity and/or query coverage percentage or the absence of any sequence classification result, even when compared to the complete ‘Nucleotide’ Genbank database. The results of the taxonomic assignment to vascular plants are presented in Supplementary Table S1. The OTU sequences were assigned to plant taxa with at least 95% identity and coverage, from which 70% of the OTUs had ≥ 98% sequence identity with the assigned taxa. The positive control of the DNA extraction, Corylus avellana pollen, was correctly identified after HTS. From the 19 negative controls included in the extraction plate, one negative control was selected for sequencing, the only one with sufficient amplicon concentration (2 ng μl−1). In this sample two OTUs were detected (263,649 reads), both assigned to Quercus spp. and contributing  More

1.Namita, P., Mukesh, R. & Vijay, K. J. Camellia Sinensis (Green Tea): A review. Glob. J. Pharmacol. 6(2), 52–59 (2012).
Google Scholar 
2.Chang, K. World Tea Production and Trade. Current and Future Development (FAO, Rome, 2015).
Google Scholar 
3.Chang, K. & Brattlof, M. World Tea Production and Trade. Current and Future Development (FAO, 2015).
Google Scholar 
4.Kochlamazashvili, I. & Kakulia, N. The Georgian Tea Sector: A Value Chain Study. ISET Policy Institute. Study prepared in the framework of ENPARD project Cooperation for Rural Prosperity in Georgia (2015).5.Lesica, P., McCune, B., Cooper, S. V. & Hong, W. S. Differences in lichen and bryophyte communities between old-growth and managed second-growth forests in the Svan Valley Montana. Can. J. Bot. 69, 1745–1755 (1991).Article 

Google Scholar 
6.Nowak, A., Plášek, V., Nobis, M. & Nowak, S. Epiphytic communities of open habitats in the Western Tian-Shan Mts (Middle Asia: Kyrgyzstan). Cryptog. Bryol. 37(4), 415–433 (2016).Article 

Google Scholar 
7.Rhoades, F. M. Nonvascular epiphytes in forest canopies: Worldwide distribution, abundance and ecological roles. In Forest Canopies (eds. Lowman, M.D. & Nadkarni, N. M.) 353–408 (1995).8.Haines, W. P. & Renwick, J. A. A. Bryophytes as food: Comparative consumption and utilization of mosses by a generalist insect herbivore. Entomol Exp Appl. 133, 296–306. https://doi.org/10.1111/j.1570-7458.2009.00929.x (2009).Article 

Google Scholar 
9.Kuřavová, K. et al. Is feeding on mosses by groundhoppers in the genus Tetrix (Insecta: Orthoptera) opportunistic or selective?. Arthropod-Plant Int. 11, 35–43. https://doi.org/10.1007/s11829-016-9461-9 (2017).Article 

Google Scholar 
10.Matuszkiewicz, W. Przewodnik do Oznaczania Zbiorowisk Roślinnych Polski (Wyd Nauk, PWN, 2001).
Google Scholar 
11.Krestov, P. V. Forest vegetation of easternmost Russia (Russian Far East). In Forest Vegetation of Northeast Asia (eds Kolbek, J. et al.) 93–180 (Springer, 2003).Chapter 

Google Scholar 
12.Kuznetsov, O. Topology-ecological classification of mire vegetation in the Republic of Karelia (Russia). In Biodiversity and Conservation of Boreal Nature. Proceedings of the 10 years anniversary symposium of the Nature Reserve Friendship (eds Heikkilä, R. & Lindholm, T.) 117–123 (Elsevier, 2003).
Google Scholar 
13.Černý, T. Phytosociological Study of Selected Critical Thermophilous Vegetation Complexes in the Czech Republic. A thesis submitted for the degree of Doctor of Philosophy in the Department of Botany Faculty of Sciences, Charles University (2007).14.Chytrý, M. et al. A modern analogue of the Pleistocene steppe-tundra ecosystem in southern Siberia. Boreas 48, 36–56 (2019).Article 

Google Scholar 
15.Wolski, G. J. & Kruk, A. Determination of plant communities based on bryophytes: The combined use of Kohonen artificial neural network and indicator species analysis. Ecol. Indic 113, 106160. https://doi.org/10.1016/j.ecolind.2020.106160 (2020).Article 

Google Scholar 
16.Benzing, D. Vulnerabilities of tropical forests to climate change: The significance of resident epiphytes. Clim. Change 39, 519–540 (1998).Article 

Google Scholar 
17.Gustafsson, L., Fiskesjö, A., Ingelög, T., Petterson, B. & Thor, G. Factors of importance to some lichen species of deciduous broad-leaved woods in southern Sweden. Lichenologist 24, 255–266 (1992).Article 

Google Scholar 
18.Frahm, J. P. Ecology of bryophytes along altitudinal and latitudinal gradients in Chile. Trop. Bryol. 21, 67–79 (2002).
Google Scholar 
19.Číhal, L., Kaláb, O. & Plášek, V. Modeling the distribution of rare and interesting moss species of the family Orthotrichaceae (Bryophyta) in Tajikistan and Kyrgyzstan. Acta Soc. Bot. Pol. 86(2), 3543. https://doi.org/10.5586/asbp.3543 (2017).Article 

Google Scholar 
20.Łubek, A., Kukwa, M., Czortek, P. & Jaroszewicz, B. Impact of Fraxinus excelsior dieback on biota of ash-associated lichen epiphytes at the landscape and community level. Biodivers. Conserv. 29, 431–450. https://doi.org/10.1007/s10531-019-01890-w (2020).Article 

Google Scholar 
21.Łubek, A., Kukwa, M., Jaroszewicz, B. & Czortek, P. Identifying mechanisms shaping lichen functional diversity in a primeval forest. For. Ecol. Manag. 475, 118434. https://doi.org/10.1016/j.foreco.2020.118434 (2020).Article 

Google Scholar 
22.Barkman, J. J. Phytosociology and Ecology of Cryptogamic Epiphytes. Including a Taxonomic Survey and Description of Their Vegetation Units in Europe, Van Gorcum, Comp (N. V Assen, 1958).
Google Scholar 
23.Green, T. G. A. & Lange, O. L. Photosynthesis in poikilohydric plants: A comparison of lichens and bryophytes. In Ecophysiology of Photosynthesis (eds Schulze, E.-D. & Caldwell, M. M.) 319–341 (Springer-Verlag, 1995).Chapter 

Google Scholar 
24.Scheidegger, C., Wolseley, P. A. & Landolt, R. Towards conservation of lichens. Forest. Snow Landsc. Res. 75, 285–433 (2000).
Google Scholar 
25.Tønsberg, T. & Høiland, K. A study of the macrolichen flora on the sand-dune areas on Lista, SW Norway. Nor. J. Bot. 27, 131–134 (1980).
Google Scholar 
26.Thiet, R. K., Doshas, A. & Smith, S. M. Effects of biocrusts and lichen-moss mats on plant productivity in a US sand dune ecosystem. Plant Soil 377(1), 235–244 (2014).CAS 
Article 

Google Scholar 
27.Vaz, A. S., Marques, J. & Honrado, J. P. Patterns of lichen diversity in coastal sand-dunes of northern Portugal. Bot. Complut. 38, 89–96 (2014).Article 

Google Scholar 
28.Antoninka, A., Bowker, M. A., Reed, S. C. & Doherty, K. Production of greenhouse-grown biocrust mosses and associated cyanobacteria to rehabilitate dryland soil function. Restor. Ecol. 24(3), 324–335 (2016).Article 

Google Scholar 
29.Jüriado, I., Kämärä, M.-L. & Oja, E. Environmental factors and ground disturbance affecting the composition of species and functional traits of ground layer lichens on grey dunes and dune heaths of Estonia. Nord. J. Bot. 34(2), 244–255 (2016).Article 

Google Scholar 
30.Balogh, R. et al. Mosses and lichens in dynamics of acidic sandy grasslands: Specific response to grazing exclosure. Acta Biol. Plant. Agriensis 5(1), 30 (2017).
Google Scholar 
31.Concostrina-Zubiri, L., Arenas, J. M., Martínez, I. & Escudero, A. Unassisted establishment of biological soil crusts on dryland road slopes. Web Ecol. 19(1), 39–51 (2019).Article 

Google Scholar 
32.Kubiak, D. & Oszyczka, P. Non-forested vs forest environments: The effect of habitat conditionson host tree parameters and the occurrence of associated epiphytic lichens. Fungal Ecol. 47, 100957 (2020).Article 

Google Scholar 
33.Gradstein, S. R. & Sporn, S. G. Land-use change and epiphytic bryophyte diversity in the Tropics. Nova Hedwigia 138, 311–323 (2010).
Google Scholar 
34.Guevara, S., Purata, S. E. & Van der Maarel, E. The role of remnant forest trees in tropical secondary succession. Vegetatio 66, 77–84 (1986).
Google Scholar 
35.Sillett, S. C., Gradstein, S. R. & Griffin, D. Bryophyte diversity of Ficus tree crowns from cloud forest and pasture in Costa Rica. Bryologist 98(2), 251–260 (1995).Article 

Google Scholar 
36.Werner, F., Homeier, J. & Gradstein, S. R. Diversity of vascular epiphytes on isolated remnant trees in the montane forest belt of southern Ecuador. Ecotropica 11, 21–40 (2005).
Google Scholar 
37.Lara, F., Garilleti, R. & Mazimpaka, V. Orthotrichum karoo (Orthotrichaceae), a new species with hyaline-awned leaves from southwestern Africa. Bryologist 112(1), 194–201 (2009).Article 

Google Scholar 
38.Lara, F. & Mazimpaka, V. Ma´s sobre la presencia de Orthotrichum acuminatum en la Península Ibérica. Cryptog. Bryol. Lichenol. 13(4), 349–354 (1992).
Google Scholar 
39.Garilleti, R., Lara, F. & Mazimpaka, V. Orthotrichum anodon (Orthotrichaceae, Bryopsida), a new species from California, and its relationships with other Orthotricha sharing puckered capsule mouths. Bryologist 109(2), 188–196 (2006).Article 

Google Scholar 
40.Hallingbäck, T. & Hodgetts, N. Mosses Liverworts and Hornworts. Status survey and conservation action plan for bryophytes (Cambridge University Press, 2000).
Google Scholar 
41.Belinchón, R., Martínez, I., Escudero, A., Aragón, G. & Valladares, F. Edge effects on epiphytic communities in a Mediterranean Quercus pyrenaica forest. J. Veg. Sci. 18, 81–90. https://doi.org/10.1111/j.1654-1103.2007.tb02518.x (2007).Article 

Google Scholar 
42.Boudreault, C., Gauthier, S. & Bergeron, Y. Epiphytic lichens and bryophytes on Populus Tremuloides along a chronosequence in the Southwestern Boreal Forest of Quebec, Canada. Bryologist 103, 725–738. https://doi.org/10.1639/0007-2745(2000)103[0725:ELABOP]2.0.CO;2 (2009).Article 

Google Scholar 
43.Rambo, T. Structure and composition of corticolous epiphyte communities in a Sierra Nevada old-growth mixed-conifer forest. Bryologist 113, 55–71. https://doi.org/10.1639/0007-2745-113.1.55 (2010).Article 

Google Scholar 
44.Plášek, V., Nowak, A., Nobis, M., Kusza, G. & Kochanowska, K. Effect of 30 years of road traffic abandonment on epiphytic moss diversity. Environ. Monit. Assess. 186, 8943–8959. https://doi.org/10.1007/s10661-014-4056-3 (2014).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
45.Skoupá, Z., Ochyra, R., Guo, S. L., Sulayman, M. & Plášek, V. Distributional novelties for Lewinskya, Nyholmiella and Orthotrichum (Orthotrichaceae) in China. Herzogia 30, 58–73. https://doi.org/10.13158/heia.30.1.2017.58 (2017).Article 

Google Scholar 
46.Skoupá, Z., Ochyra, R., Guo, S.-L., Sulayman, M. & Plášek, V. Three remarkable additions of Orthotrichum species (Orthotrichaceae) to the moss flora of China. Herzogia 31, 88–100. https://doi.org/10.13158/099.031.0105 (2018).Article 

Google Scholar 
47.Gradstein, R. et al. Bryophytes of Mount Patuha, West Java, Indonesia. Reinwardtia 13(2), 107–123 (2010).
Google Scholar 
48.Saat, A., Talib, M. S., Harun, N., Hamzah, Z. & Wood, A. K. Spatial variability of arsenic and heavy metals in a highland tea plantation using lichens and mosses as bio-monitors. Asian J. Nat. Appl. Sci. 5(1), 10–21 (2016).
Google Scholar 
49.Fick, S. E. & Hijmans, R. J. WorldClim 2: New 1km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37(12), 4302–4315 (2017).Article 

Google Scholar 
50.Wirth, V. Ökologische Zeigerwerte von Flechten. Herzogia 23(2), 229–248 (2010).Article 

Google Scholar 
51.Ellenberger, H. et al. Zeigerwerte von Planzen in Mitteleuropa. Scr. Geobot. 18, 1–248 (1991).
Google Scholar 
52.Smith, C. W. et al. The Lichens of Great Britain and Ireland 1046 (British Lichen Society, 2009).
Google Scholar 
53.Hodgetts, N. et al. An annotated checklist of bryophytes of Europe, Macaronesia and Cyprus. J. Bryol. 42(1), 1–116. https://doi.org/10.1080/03736687.2019.1694329 (2020).Article 

Google Scholar 
54.Pancho, J. V. Some bryophytes in tea plantations, Pagilaran Central Java. Biotrop. Bull. 11, 279–282 (1979).
Google Scholar 
55.Tan, B. C. et al. Mosses of Gunung Halimun National Park, West Java, Indonesia. Reinwardtia 12, 205–214 (2006).
Google Scholar 
56.Ohsawa, M. Weeds of tea plantations. In Biology and Ecology of Weeds. Geobotany Vol. 2 (eds Holzner, W. & Numata, M.) (Springer, 1982).
Google Scholar 
57.Gradstein, R. et al. Bryophytes of Mount Patuha, West Java, Indonesia. Reinwardtia 13, 107–123 (2010).
Google Scholar 
58.Whitelaw, M. & Burton, M. A. S. Diversity and distribution of epiphytic bryophytes on Bramley’s Seedling trees in East of England apple orchards. Glob. Ecol. Conserv. 4, 380–387. https://doi.org/10.1016/j.gecco.2015.07.014 (2015).Article 

Google Scholar 
59.Söderström, L. Bryophytes and decaying wood – a comparison between manager and natural forest. Holarc. Ecol. 14, 121–130 (1991).
Google Scholar 
60.Cieśliński, S. et al. Relikty lasu puszczańskiego, In Białowieski Park Narodowy (1921–1996) w badaniach geobotanicznych. Phytocoenosis, 8 (N.S.), Seminarium Geobotanicum (ed. Faliński, J. B.) 4, 47–64 (1996).61.Vanderpoorten, A., Engels, P. & Sotiaux, A. Trends in diversity and abundance of obligate epiphytic bryophytes in a highly managed landscape. Ecography 27, 567–576 (2004).Article 

Google Scholar 
62.Ódor, P., van Dort, K., Aude, E., Heilmann-Clausen, J. & Christensen, M. Diversity and composition of dead wood inhabiting bryophyte communities in European beech forest. Biol. Soc. Esp. Briol. 26–27, 85–102 (2005).
Google Scholar 
63.Friedel, A., Oheimb, G. V., Dengler, J. & Härdtle, W. Species diversity and species composition of epiphytic bryophytes and lichens: A comparison of managed and unmanaged beech forests in NE Germany. Feddes Repert. 117(1–2), 172–185 (2006).Article 

Google Scholar 
64.Wolski, G. J. Siedliskowe Uwarunkowania Występowania Mszaków w Rezerwatach Przyrody Chroniących Jodłę Pospolitą w Polsce Środkowej (Praca doktorska wykonana w Katedrze Geobotaniki i Ekologii Roślin UŁ, 2013).
Google Scholar 
65.Fudali, E. & Wolski, G. J. Ecological diversity of bryophytes on tree trunks in protected forests (a case study from Central Poland). Herzogia 28(1), 91–107 (2015).Article 

Google Scholar 
66.Shi, X.-M. et al. Epiphytic bryophytes as bio-indicators of atmospheric nitrogen deposition in a subtropical montane cloud forest: Response patterns, mechanism, and critical load. Environ. Pollut. 229, 932–941. https://doi.org/10.1016/j.envpol.2017.07.077 (2017).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
67.Cornelissen, J. H. C. & Gradstein, S. R. On the occurrence of bryophytes and macrolichens in different lowland rain forest types of Mabura Hill, Guyana. Trop. Bryol. 3, 29–35. https://doi.org/10.11646/bde.3.1.4 (1990).Article 

Google Scholar 
68.Lyons, B., Nadkarni, N. M. & North, M. P. Spatial distribution and succession of epiphytes on Tsuga heterophylla (western hemlock) in an old-growth Douglas-fir forest. Can. J. Bot. 78(7), 957–968. https://doi.org/10.1139/cjb-78-7-957 (2000).Article 

Google Scholar 
69.Cornelissen, J. H. C. & Steege, H. T. Distribution and ecology of epiphytic bryophytes and lichens in dry evergreen forest of Guyana. J. Trop. Ecol. 5, 131–150. https://doi.org/10.1017/S0266467400003400 (1989).Article 

Google Scholar 
70.Woods, C. L., Cardelús, C. L., Dewalt, S. J. & Piper, F. Microhabitat associations of vascular epiphytes in a wet tropical forest canopy. J. Ecol. 103(2), 421–430. https://doi.org/10.1111/1365-2745.12357 (2015).Article 

Google Scholar 
71.Sporn, S. G., Bos, M. M., Kessler, M. & Gradstein, S. R. Vertical distribution of epiphytic bryophytes in an Indonesian rainforest. Biodivers. Conserv. 19(3), 745–760. https://doi.org/10.1007/s10531-009-9731-2 (2010).Article 

Google Scholar 
72.Czerepko, J. et al. How sensitive are epiphytic and epixylic cryptogams as indicators of forest naturalness? Testing bryophyte and lichen predictive power in stands under different management regimes in the Białowieża forest. Ecol. Indic. 125, 107532. https://doi.org/10.1016/j.ecolind.2021.107532 (2021).Article 

Google Scholar 
73.Putna, S. & Mězaka, A. Preferences of epiphytic bryophytes for forest stand and substrate in North-East Latvia. Folia Cryptog. Estonica 51, 75–83 (2014).Article 

Google Scholar 
74.Manakyan, V. A. Results of bryological studies in Armenia. Arctoa 5, 15–33 (1995).Article 

Google Scholar 
75.Redfearn, P. L., Tan, B. C. & He, S. A newly updated and annotated checklist of Chines mosses. J. Hattori Bot. Lab. 79, 163–357 (1996).
Google Scholar 
76.Kürschner, H. Bryophyte Flora of the Arabian Peninsula and Socotra. Bryophytorum Bibliotheca (JCramer in der Gebrüder Borntraeger Verlagsbuchhandlung, 2000).
Google Scholar 
77.Higuchi, M. & Nishimura, N. Mosses of Pakistan. J. Hattori Bot. Lab. 93, 273–291 (2003).
Google Scholar 
78.Ignatov, M. S., Afonina, O. M. & Ignatova, E. A. Check-list of mosses of East Europe and North Asia. Arctoa 15, 1–130. https://doi.org/10.15298/arctoa.15.01 (2006).Article 

Google Scholar 
79.Sabovljević, M. et al. Check-list of the mosses of SE Europe. Phytol. Balcan. 14(2), 207–244 (2008).
Google Scholar 
80.Dandotiya, D., Govindapyari, H., Suman, S. & Uniyal, P. L. Checklist of the bryophytes of India. Arch. Bryol. 88, 71–72 (2011).
Google Scholar 
81.Hodgetts, N. G. Checklist and Country Status of European bryophytes—Towards a New Red List for Europe. Irish Wildlife Manuals, No. 84. (National Parks and Wildlife Service, Department of Arts, Heritage and the Gaeltacht, 2011). https://www.hdl.handle.net/2262/73373.82.Kürschner, H. & Frey, W. Liverworts, Mosses and Hornworts of Southwest Asia (Marchantiophyta, Bryophyta, Anthoceroptophyta). Nova Hedwigia 139, 179–180 (2011).
Google Scholar 
83.Suzuki, T. A revised new catalog of the mosses of Japan. Hattoria 7, 9–223. https://doi.org/10.18968/hattoria.7.0_9 (2016).Article 

Google Scholar 
84.Kürschner, H. & Frey, W. Liverworts, mosses and hornworts of Afghanistan—our present knowledge. Acta Mus. Siles. Sci. Natur. 68, 11–24 (2019).
Google Scholar 
85.Brotherus, V. F. Enumeratio muscorum Caucasi. Acta Soc. Sci. Fenn. 19, 1–170 (1892).
Google Scholar 
86.Chikovani, N. & Svanidze, T. Checklist of bryophyte species of Georgia. Braun-Blanquetia 34, 97–116. https://doi.org/10.13158/heia.26.1.2013.213 (2004).Article 

Google Scholar 
87.Doroshina, G. Y. New moss records from Georgia. 1. Arctoa 19, 281 (2010).
Google Scholar 
88.Sohrabi, M., Ahti, T. & Urbanavichus, G. Parmelioid lichens of Iran and the caucasus Region. Mycol. Balc. 4, 21–30 (2007).
Google Scholar 
89.Hawksworth, D. L., Blanco, O., Divakar, P. K., Ahti, T. & Crespo, A. A first checklist of parmelioid and similar lichens in Europe and some adjacent territories, adopting revised generic circumscriptions and with indications of species distributions. Lichenologist 40(1), 1–21. https://doi.org/10.1017/S0024282908007329 (2008).Article 

Google Scholar 
90.Syrek, M. & Kukwa, M. Taxonomy of the lichen Cladonia rei and its status in Poland. Biologia 63(4), 493–497. https://doi.org/10.2478/s11756-008-0092-1 (2008).Article 

Google Scholar 
91.Burgaz, A. R., Ahti, T., Inashvili, T., Batsatsashvili, K. & Kupradze, I. Study of georgian Cladoniaceae. Bot. Complut. 42, 19–55. https://doi.org/10.5209/BOCM.61367 (2018).Article 

Google Scholar 
92.Fałtynowicz, W. The lichens, lichenicolous and allied fungi of Poland. An annotated checklist. In Biodiversity of Poland (ed. Mirek, A.) 1–435 (W. Szafer Institute of Botany, Polish Academy of Sciences, 2003).
Google Scholar 
93.Plášek, V., Sawicki, J., Ochyra, R., Szczecińska, M. & Kulik, T. New taxonomical arrangement of the traditionally conceived genera Orthotrichum and Ulota (Orthotrichaceae, Bryophyta). Acta Mus. Sil. 64, 169–174. https://doi.org/10.1515/cszma-2015-0024 (2015).Article 

Google Scholar 
94.Lara, F. et al. Lewinskya, a new genus to accommodate the phaneroporous and monoicous taxa of Orthotrichum (Bryophyta, Orthotrichaceae). Cryptog. Bryol. 37, 361–382. https://doi.org/10.7872/cryb/v37.iss4.2016.361 (2016).Article 

Google Scholar 
95.Sawicki, J. et al. Mitogenomic analyses support the recent division of the genus Orthotrichum (Orthotrichaceae, Bryophyta). Sci. Rep. 7, 4408. https://doi.org/10.1038/s41598-017-04833-z (2017).ADS 
CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
96.Kürschner, H., Batsatsashvili, K. & Parolly, G. Noteworthy additions to the bryophyte flora of Georgia. Herzogia 26, 213–216. https://doi.org/10.13158/heia.26.1.2013.213 (2013).Article 

Google Scholar 
97.Ellis, L. T. et al. New national and regional bryophyte records, 49. J. Bryol. 38(4), 327–347 (2016).Article 

Google Scholar 
98.Ellis, L. T. et al. New national and regional bryophyte records, 51. J. Bryol. 39(2), 177–190 (2017).Article 

Google Scholar 
99.Eckstein, J., Garilleti, R. & Lara, F. Lewinskya transcaucasica (Orthotrichaceae, Bryopsida) sp. nov. A contribution to the bryophyte flora of Georgia. J. Bryol. 40(1), 31–38. https://doi.org/10.1080/03736687.2017.1365218 (2018).Article 

Google Scholar 
100.Eckstein, J. & Zündorf, H.-J. Orthotrichaceous mosses (Orthotricheae, Orthotrichaceae) of the Genera Lewinskya, Nyholmiella, Orthotrichum, Pulvigera and Ulota Contributions to the bryophyte flora of Georgia 1. Cryptog. Bryol. 38(4), 365–382. https://doi.org/10.7872/cryb/v38.iss4.2017.365 (2017).Article 

Google Scholar 
101.Schäfer-Verwimp, A. Orthotrichum Hedw. In Die Moose Baden-Württembergs. Band 2: Spezieller Teil (Bryophytina II, Schistostegales bis Hypnobryales) (eds Nebel, M. & Philippi, G.) 170–197 (Eugen Ulmer, 2001).
Google Scholar 
102.Lara, F. & Garilleti, R. Orthotrichum Hedw. In Flora briofítica Ibérica (eds Guerra, J. & Brugués, C. M.) 50–135 (Universidad de Murcia Sociedad Española de Briología, 2014).
Google Scholar 
103.Lewinsky, J. The genus Orthotrichum Hedw. (Orthotrichaceae, Musci) in Southeast Asia. A taxonomic revision. J. Hattori Bot. Lab. 72, 1–88 (1992).
Google Scholar 
104.Schäfer-Verwimp, A. & Gruber, J. P. Orthotrichum (Orthotrichaceae, Bryopsida) in Pakistan. Trop. Bryol. 21, 1–9. https://doi.org/10.11646/bde.21.1.2 (2002).Article 

Google Scholar 
105.Draper, I., Mazimpaka, V., Albertos, B., Garilleti, R. & Lara, F. A survey of the epiphytic bryophyte flora of the Rif and Tazzeka Mountains (northern Morocco). J. Bryol. 27, 23–34. https://doi.org/10.1179/174328205X40554 (2005).Article 

Google Scholar 
106.Brassard, G. R. Orthotrichum stramineum new to North America. Bryologist 87, 168 (1984).Article 

Google Scholar 
107.Lewinsky-Haapasaari, J. & Long, D. G. Orthotrichum stramineum Hornsch. new to China. J. Bryol. 19, 350–352. https://doi.org/10.1179/jbr.1996.19.2.350 (1996).Article 

Google Scholar 
108.Plášek, V. et al. A synopsis of Orthotrichum s. lato (Bryophyta, Orthotrichaceae) in China, with distribution maps and a key to determination. Plants 10, 499. https://doi.org/10.3390/plants10030499 (2021).Article 
PubMed 
PubMed Central 

Google Scholar  More

1.Stein, A., Gerstner, K. & Kreft, H. Environmental heterogeneity as a universal driver of species richness across taxa, biomes and spatial scales. Ecol. Lett. 17, 866–880 (2014).PubMed 
Article 

Google Scholar 
2.Tews, J. et al. Animal species diversity driven by habitat heterogeneity/diversity: The importance of keystone structures—Animal species diversity driven by habitat heterogeneity. J. Biogeogr. 31, 79–92 (2004).Article 

Google Scholar 
3.Graham, N. A. J. & Nash, K. L. The importance of structural complexity in coral reef ecosystems. Coral Reefs 32, 315–326 (2013).ADS 
Article 

Google Scholar 
4.Reimchen, T. E. Substratum heterogeneity, crypsis, and colour polymorphism in an intertidal snail (Littorina mariae). Can. J. Zool. 57, 1070–1085 (1979).Article 

Google Scholar 
5.Petren, K. & Case, T. J. Habitat structure determines competition intensity and invasion success in gecko lizards. Proc. Natl. Acad. Sci. 95, 11739–11744 (1998).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
6.Gratwicke, B. & Speight, M. R. The relationship between fish species richness, abundance and habitat complexity in a range of shallow tropical marine habitats. J. Fish Biol. 66, 650–667 (2005).Article 

Google Scholar 
7.Williams, S. E., Marsh, H. & Winter, J. Spatial scale, species diversity, and habitat structure: Small mammals in Australian tropical rain forest. Ecology 83, 1317–1329 (2002).Article 

Google Scholar 
8.Renoult, J. P., Kelber, A. & Schaefer, H. M. Colour spaces in ecology and evolutionary biology. Biol. Rev. 92, 292–315 (2017).PubMed 
Article 

Google Scholar 
9.Cuthill, I. C. et al. The biology of color. Science 357, eaan0221 (2017).PubMed 
Article 
CAS 

Google Scholar 
10.Guilford, T. & Dawkins, M. S. Receiver psychology and the evolution of animal signals. Anim. Behav. 42, 1–14 (1991).Article 

Google Scholar 
11.Crook, A. C. Colour patterns in a coral reef fish is background complexity important?. J. Exp. Mar. Biol. Ecol. 217, 237–252 (1997).Article 

Google Scholar 
12.Marshall, J. Communication and camouflage with the same ‘bright’ colours in reef fishes. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 355, 1243–1248 (2000).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
13.Seehausen, O. et al. Speciation through sensory drive in cichlid fish. Nature 455, 620–626 (2008).ADS 
CAS 
PubMed 
Article 

Google Scholar 
14.Wilkins, L., Marshall, N. J., Johnsen, S. & Osorio, D. Modelling colour constancy in fish: Implications for vision and signalling in water. J. Exp. Biol. 219, 1884–1892 (2016).PubMed 

Google Scholar 
15.Osorio, D. & Vorobyev, M. A review of the evolution of animal colour vision and visual communication signals. Vis. Res. 48, 2042–2051 (2008).CAS 
PubMed 
Article 

Google Scholar 
16.Caley, J. & St John, J. Refuge availability structures assemblages of tropical reef fishes. J. Anim. Ecol. 45, 414–428 (1996).Article 

Google Scholar 
17.Connolly, S. R., Hughes, T. P., Bellwood, D. R. & Karlson, R. H. Community structure of corals and reef fishes at multiple scales. Science 309, 1363–1365 (2005).ADS 
CAS 
PubMed 
Article 

Google Scholar 
18.Allen, G. R. & Steene, R. Indo-Pacific Coral Reef Field Guide (Tropical Reef Research, 1994).
Google Scholar 
19.Bellwood, D. R. Regional-scale assembly rules and biodiversity of coral reefs. Science 292, 1532–1535 (2001).ADS 
CAS 
PubMed 
Article 

Google Scholar 
20.Humann, P., DeLoach, N., Allen, G. & Steene, G. Reef Fish Identification: Tropical Pacific (New World Publications, 2015).
Google Scholar 
21.Barneche, D. R. et al. Body size, reef area and temperature predict global reef-fish species richness across spatial scales. Glob. Ecol. Biogeogr. 28, 315–327 (2019).Article 

Google Scholar 
22.Brandl, S. J., Goatley, C. H. R., Bellwood, D. R. & Tornabene, L. The hidden half: ecology and evolution of cryptobenthic fishes on coral reefs: Cryptobenthic reef fishes. Biol. Rev. 93, 1846–1873 (2018).PubMed 
Article 

Google Scholar 
23.Carr, M. H., Anderson, T. W. & Hixon, M. A. Biodiversity, population regulation, and the stability of coral-reef fish communities. Proc. Natl. Acad. Sci. 99, 11241–11245 (2002).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
24.Hixon, M. A. 60 years of coral reef fish ecology: Past, present, future. Bull. Mar. Sci. 87, 727–765 (2011).Article 

Google Scholar 
25.Stuart-Smith, R. D. et al. Integrating abundance and functional traits reveals new global hotspots of fish diversity. Nature 501, 539–542 (2013).ADS 
CAS 
PubMed 
Article 

Google Scholar 
26.Froese, R. & Pauly, D. FishBase. World Wide Web electronic publication. http://www.fishbase.org (2019).27.Marshall, N. J., Jennings, K., McFarland, W. N., Loew, E. R. & Losey, G. S. Visual biology of Hawaiian coral reef fishes. II. Colors of Hawaiian coral reef fish. Copeia 2003, 455–466 (2003).Article 

Google Scholar 
28.Merilaita, S. Visual background complexity facilitates the evolution of camouflage. Evolution 57, 1248–1254 (2003).PubMed 
Article 

Google Scholar 
29.Matz, M. V., Lukyanov, K. A. & Lukyanov, S. A. Family of the green fluorescent protein: Journey to the end of the rainbow. BioEssays 24, 953–959 (2002).CAS 
PubMed 
Article 

Google Scholar 
30.Alieva, N. O. et al. Diversity and evolution of coral fluorescent proteins. PLoS ONE 3, e2680 (2008).ADS 
PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
31.Salih, A., Larkum, A., Cox, G., Kühl, M. & Hoegh-Guldberg, O. Fluorescent pigments in corals are photoprotective. Nature 408, 850–853 (2000).ADS 
CAS 
PubMed 
Article 

Google Scholar 
32.Veron, J., Stafford-Smith, M., DeVantier, L. & Turak, E. Overview of distribution patterns of zooxanthellate Scleractinia. Front. Mar. Sci. 1, 81 (2015).Article 

Google Scholar 
33.Matz, M. V., Marshall, N. J. & Vorobyev, M. Are corals colorful?. Photochem. Photobiol. 82, 345 (2006).CAS 
PubMed 
Article 

Google Scholar 
34.Marshall, N. J., Jennings, K., McFarland, W. N., Loew, E. R. & Losey, G. S. Visual biology of Hawaiian coral reef fishes. III. Environmental light and an integrated approach to the ecology of reef fish vision. Copeia 2003, 467–480 (2003).Article 

Google Scholar 
35.Neumeyer, C. Color vision in fishes and its neural basis. In Sensory Processing in Aquatic Environments (eds Collin, S. P. & Marshall, N. J.) 223–235 (Springer, 2003). https://doi.org/10.1007/978-0-387-22628-6_11.Chapter 

Google Scholar 
36.Oswald, F. et al. Contributions of host and symbiont pigments to the coloration of reef corals. FEBS J. 274, 1102–1122 (2007).CAS 
PubMed 
Article 

Google Scholar 
37.Schweikert, L. E., Fitak, R. R., Caves, E. M., Sutton, T. T. & Johnsen, S. Spectral sensitivity in ray-finned fishes: Diversity, ecology, and shared descent. J. Exp. Biol. https://doi.org/10.1242/jeb.189761 (2018).Article 
PubMed 

Google Scholar 
38.Veron, J. E. N., Stafford-Smith., M. G., Turak, E. & DeVantier, L. M. Corals of the World. www.coralsoftheworld.org (2020). Accessed April 2019.39.Weller, H. I. & Westneat, M. W. Quantitative color profiling of digital images with earth mover’s distance using the R package colordistance. PeerJ 7, e6398 (2019).PubMed 
PubMed Central 
Article 

Google Scholar 
40.Cox, K., Woods, M. & Reimchen, T. E. Coral species richness, coral hue, and reef fish richness across 74 ecoregions within four oceanic basins. Figshare https://doi.org/10.6084/m9.figshare.12317591 (2020).41.R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019).
Google Scholar 
42.The Ocean Agency & XL Catlin Seaview Survey. Coral Reef Image Bank. www.coralreefimagebank.org (2019). Accessed April 2019.43.Choat, J. H. & Bellwood, D. R. Reef fishes: Their history and evolution. In The Ecology of Fishes on Coral Reefs (ed. Sale, P. F.) 39–66 (Academic Press, 1991).Chapter 

Google Scholar 
44.Jones, G. P., Barone, G., Sambrook, K. & Bonin, M. C. Isolation promotes abundance and species richness of fishes recruiting to coral reef patches. Mar. Biol. 167, 1–13 (2020).Article 
CAS 

Google Scholar 
45.Lirman, D. et al. Severe 2010 cold-water event caused unprecedented mortality to corals of the florida reef tract and reversed previous survivorship patterns. PLoS ONE 6, e23047 (2011).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
46.Habary, A., Johansen, J. L., Nay, T. J., Steffensen, J. F. & Rummer, J. L. Adapt, move or die: How will tropical coral reef fishes cope with ocean warming?. Glob. Change Biol. 23, 566–577 (2017).ADS 
Article 

Google Scholar 
47.Almany, G. R. & Webster, M. S. The predation gauntlet: Early post-settlement mortality in reef fishes. Coral Reefs 25, 19–22 (2006).ADS 
Article 

Google Scholar 
48.Brandl, S. J. et al. Demographic dynamics of the smallest marine vertebrates fuel coral reef ecosystem functioning. Science 364, 1189–1192 (2019).ADS 
CAS 
PubMed 
Article 

Google Scholar 
49.Coker, D. J., Wilson, S. K. & Pratchett, M. S. Importance of live coral habitat for reef fishes. Rev. Fish Biol. Fish. 24, 89–126 (2014).Article 

Google Scholar 
50.Coker, D. J., Pratchett, M. S. & Munday, P. L. Coral bleaching and habitat degradation increase susceptibility to predation for coral-dwelling fishes. Behav. Ecol. 20, 1204–1210 (2009).Article 

Google Scholar 
51.Sale, P. F. Maintenance of high diversity in coral reef fish communities. Am. Nat. 111, 337–359 (1977).Article 

Google Scholar 
52.Munday, P. L. Competitive coexistence of coral-dwelling fishes: The lottery hypothesis revisited. Ecology 85, 623–628 (2004).Article 

Google Scholar 
53.Hixon, M. A. Synergistic predation, density dependence, and population regulation in marine fish. Science 277, 946–949 (1997).CAS 
Article 

Google Scholar 
54.Endler, J. A. & Thery, M. Interacting effects of Lek placement, display behavior, ambient light, and color patterns in three neotropical forest-dwelling birds. Am. Nat. 148, 421–452 (1996).Article 

Google Scholar 
55.Reimchen, T. E. Shell colour ontogeny and tubeworm mimicry in a marine gastropod Littorina mariae. Biol. J. Linn. Soc. 36, 97–109 (1989).Article 

Google Scholar 
56.Sparks, J. S. et al. The covert world of fish biofluorescence: A phylogenetically widespread and phenotypically variable phenomenon. PLoS ONE 9, e83259 (2014).ADS 
PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
57.Allen, J. J., Akkaynak, D., Sugden, A. U. & Hanlon, R. T. Adaptive body patterning, three-dimensional skin morphology and camouflage measures of the slender filefish Monacanthus tuckeri on a Caribbean coral reef. Biol. J. Linn. Soc. 116, 377–396 (2015).Article 

Google Scholar 
58.Cheney, K. L., Skogh, C., Hart, N. S. & Marshall, N. J. Mimicry, colour forms and spectral sensitivity of the bluestriped fangblenny, Plagiotremus rhinorhynchos. Proc. R. Soc. B Biol. Sci. 276, 1565–1573 (2009).Article 

Google Scholar 
59.Stevens, M., Lown, A. E. & Denton, A. M. Rockpool gobies change colour for camouflage. PLoS ONE 9, e110325 (2014).ADS 
PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
60.Gilby, B. L. et al. Colour change in a filefish (Monacanthus chinensis) faced with the challenge of changing backgrounds. Environ. Biol. Fishes 98, 2021–2029 (2015).Article 

Google Scholar 
61.Barnett, J. B. & Cuthill, I. C. Distance-dependent defensive coloration. Curr. Biol. 24, R1157–R1158 (2014).CAS 
PubMed 
Article 

Google Scholar 
62.Vega Thurber, R. L. et al. Chronic nutrient enrichment increases prevalence and severity of coral disease and bleaching. Glob. Change Biol. 20, 544–554 (2014).ADS 
Article 

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

Google Scholar 
64.Ortiz, J.-C. et al. Impaired recovery of the great barrier reef under cumulative stress. Sci. Adv. 4, eaar6127 (2018).ADS 
PubMed 
PubMed Central 
Article 

Google Scholar 
65.Grottoli, A. G., Rodrigues, L. J. & Palardy, J. E. Heterotrophic plasticity and resilience in bleached corals. Nature 440, 1186–1189 (2006).ADS 
CAS 
PubMed 
Article 

Google Scholar 
66.Roff, G. et al. Porites and the Phoenix effect: Unprecedented recovery after a mass coral bleaching event at Rangiroa Atoll, French Polynesia. Mar. Biol. 161, 1385–1393 (2014).Article 

Google Scholar 
67.Adjeroud, M. et al. Recovery of coral assemblages despite acute and recurrent disturbances on a South Central Pacific reef. Sci. Rep. 8, 1–8 (2018).ADS 
CAS 
Article 

Google Scholar 
68.Tittensor, D. P. et al. Global patterns and predictors of marine biodiversity across taxa. Nature 466, 1098–1101 (2010).ADS 
CAS 
PubMed 
Article 

Google Scholar 
69.Soetaert, K. plot3D: Plotting Multi-Dimensional Data R package version 1.4. https://CRAN.R-project.org/package=plot3D (2021).70.Sarkar, D. Lattice: Multivariate Data Visualization with R (Springer, 2008).MATH 
Book 

Google Scholar 
71.Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2016).MATH 
Book 

Google Scholar 
72.Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
73.Centore, P. sRGB centroids for the ISCC-NBS colour system. Munsell Colour Sci. Paint. 21, 1–21 (2016).
Google Scholar 
74.Kelly, K. L. Central notations for the revised ISCC-NBS color-name blocks. J. Res. Natl. Bur. Stand. 61, 427 (1958).Article 

Google Scholar 
75.Viechtbauer, W. Conducting meta-analyses in R with the metafor package. J. Stat. Softw. 36, 1–48 (2010).Article 

Google Scholar  More

BOOK REVIEW
13 September 2021

Marauding elephants, menacing macaques and epicurean bears

As humans encroach on the habitat of wild animals, is it any surprise that they advance upon ours?

Josie Glausiusz

0

Josie Glausiusz

Josie Glausiusz is a science journalist in Israel.Twitter: @josiegz

View author publications

You can also search for this author in PubMed
 Google Scholar

Share on Twitter
Share on Twitter

Share on Facebook
Share on Facebook

Share via E-Mail
Share via E-Mail

Download PDF

An adult male elephant wanders through the town of Siliguri, India, in February 2016.Credit: Diptendu Dutta/AFP/Getty

Fuzz: When Nature Breaks the Law Mary Roach W. W. Norton (2021)On 8 September 1488, the French fiefdom of Beaujeu issued an unusual order. Curates were charged with warning slugs three times “to cease from vexing the people by corroding and consuming the herbs of the fields and the vines, and to depart”. Mary Roach cites this episode in her introduction to Fuzz: When Nature Breaks the Law — eliciting the first laugh of many in a book in which she turns her deft wit on the destruction and death that results from human–wildlife conflict. It is a fitting sequel to her previous ‘science-ofs’: Stiff (about cadavers), Spook (the afterlife), Bonk (sex), Gulp (eating) and Grunt (combat).Beyond medieval proceedings against slugs, caterpillars and weevils, Roach addresses more modern resolutions to our rivalry with species that “regularly commit acts that put them at odds with humans”. Travelling from the alleyways of Aspen, Colorado, where epicurean bears forage among restaurant dustbins, to “leopard-terrorized hamlets” in the Himalayas, she investigates how wild creatures from cougars to crows menace humans, their crops and their property.Fundamentally, she asks: when we encroach on the habitat of wild creatures, is it any surprise that they advance on ours? Perhaps nowhere is this collision clearer than in the Indian region of North Bengal, where, each year, dozens of people die after elephant attacks. Elephants there forage at night and sleep by day in patches of teak and red sandalwood trees, the remnants of forests that once stretched from the state of Assam to the eastern border of Nepal. This elephant corridor was fractured by imperialist-era tea estates and more recently by military bases. As the population of elephants in the remaining pockets spikes, the animals are wandering into villages, eating crops and grain stores.
The long goodbye
A bull elephant in must — the periodic hormonal tumult signified by frequent erections and ogling eyeballs — is highly aggressive and can crush people. Roach accompanies researchers from the Wildlife Institute of India in Dehradun to visit “awareness camps”, where they teach villagers to stay calm and call the local Elephant Squad so that rangers can herd roving elephants back into the forest. Even better, conservationist Dipanjan Naha tells her, would be to install seismic sensors to warn of approaching elephant footfalls. But, as one officer notes: “We are disturbing them.”In India, where in Hindu tradition elephants are the incarnation of the god Ganesha, it is customary to offer compensation to the families of those killed by elephants, and by leopards. In the United States, by contrast, the focus is not on compensation but on euthanizing the few bears who attack and kill humans. With bears, too, habitat fragmentation as well as climate change appear to play a major part in the conflict with humans. Major highways on the US–Canada border might restrict the movement of black bears. In California, drought is pushing bears into urban areas and, during a record-breaking heatwave earlier this year, into the waters of Lake Tahoe.

Pushed into urban areas by encroaching development, bears raid bins for food.Credit: Tomas Hulik ARTpoint/Shutterstock

Once upon a time, bears in the forests around Aspen, Colorado, dined well on acorns, chokecherries and “the outrageous fecundity of crabapple trees”. Roach watches them in the wee hours gorging instead on crab legs and cabbage leaves, tossed out by the city’s restaurants. Stewart Breck at the National Wildlife Research Center in Fort Collins, Colorado, argues that limiting the availability of human food can reduce the need to kill or ward off marauding bears. But replacing busted bear-resistant dumpsters, hiring staff to enforce bin-locking laws, and issuing tickets to restaurants and “alpha residents” who ignore local waste-disposal ordinances isn’t easy: “the county is home to about as many billionaires as bears,” Roach writes.Complex trade-offsOften, it’s our meddling that created the threat in the first place, as when humans introduce animals that inflict unbridled harm upon native species. Case in point: carnivorous stoat (Mustela erminea), that were shipped from Europe to New Zealand in the late nineteenth century to control rabbits, themselves originally imported for food and sport. Stoats, which are agile climbers and swimmers, now prey upon New Zealand’s birds, eating eggs and chicks of tree-trunk-nesting mohua (Mohoua ochrocephala), kākā (Nestor meridionalis) and yellow-crowned kākāriki (Cyanoramphus auriceps), as well as coastal-dwelling endangered hoiho (Megadyptes antipodes).
Conservation: Backyard jungles
New Zealand launched the Predator Free 2050 programme to protect native biodiversity by eradicating stoats and two other invasive predators, rats and brushtail possums (Trichosurus vulpecula). The effort relies on humane trapping as well as helicopter drops of a biodegradable toxin called 1080. The programme has led to some small predator-free havens such as Tiritiri Matangi island, but 1080 also kills deer and native kea birds (Nestor notabilis).Such trade-offs are complex, and Roach does a fine job of weighing human needs against those of pests and predators. After all, it can be ruinous for Indian villagers to have their granaries looted by elephants and dangerous for people in Delhi to be attacked by hordes of macaques. (Roach is at her most entertaining when she attempts to track down Ishwar Singh, chief wildlife warden for the Delhi government and an expert on macaque contraception. He finally answers her call with two words, “laparoscopic sterilization”, before slamming down the phone.)But the biggest pest is clearly us. As a 2020 report by the conservation group WWF shows, populations of wild mammals, birds, fish, amphibians and reptiles have dropped by 68% on average since 1970, and one million wildlife species are in danger of extinction, because of burned forests, overfished seas, and the destruction of wild areas. There’s no mirth in that.

Nature 597, 325-326 (2021)
doi: https://doi.org/10.1038/d41586-021-02484-9

Competing Interests
The author declares no competing interests.

Related Articles

Among the warriors

Conservation: Backyard jungles

The long goodbye

Down the hatch

Subjects

Ecology

Environmental sciences

Latest on:

Ecology

Pollination advantage of rare plants unveiled
News & Views 08 SEP 21

Pollinators contribute to the maintenance of flowering plant diversity
Article 08 SEP 21

Widespread woody plant use of water stored in bedrock
Article 08 SEP 21

Environmental sciences

Spacefarers, protect our planet from falling debris
Correspondence 07 SEP 21

Australian bush fires and fuel loads
Correspondence 31 AUG 21

Boost for Africa’s research must protect its biodiversity
Correspondence 31 AUG 21

Jobs

Reseacher, indefinite-term employment, RIKEN(21W19)

RIKEN
Saitama, Japan

Post-Doc : Chemical characterization and hydrogeological modeling of fractured aquifers. Application to Volvic volcanic watershed

Université Bourgogne Franche-Comté (UBFC)
BESANCON, France

Lab Manager (f/m/div)

Max Planck Institute of Biophysics (MPIBP)
Frankfurt am Main, Germany

International PhD Program in Quantum Materials

The University of British Columbia (UBC)
Vancouver, Canada More

1.Reading, C. J. et al. Are snake populations in widespread decline?. Biol. Lett. 6, 777–780 (2010).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
2.Gibbons, J. W. et al. The Global Decline of Reptiles, Déja Vu Amphibians. Bioscience 50, 653–666 (2000).Article 

Google Scholar 
3.Wilcove, D. S., Rothstein, D., Dubow, J., Phillips, A. & Losos, E. Quantifying threats to imperiled species in the United States. Bioscience 48, 607–615 (1998).Article 

Google Scholar 
4.Stenseth, N. C. et al. Ecological effects of climate fluctuations. Science 297, 1292–1296 (2002).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
5.IUCN. Wildlife in a Changing World: An Analysis of the 2008 IUCN Red List of Threatened Species. (IUCN, 2009).6.Needleman, R. K., Neylan, I. P. & Erickson, T. Potential environmental and ecological effects of global climate change on venomous terrestrial species in the wilderness. Wilderness Environ. Med. 29, 226–238 (2018).PubMed 
Article 
PubMed Central 

Google Scholar 
7.Segura, C., Feriche, M., Pleguezuelos, J. M. & Santos, X. Specialist and generalist species in habitat use: Implications for conservation assessment in snakes. J. Nat. Hist. 41, 2765–2774 (2007).Article 

Google Scholar 
8.Moreno-Rueda, G., Pleguezuelos, J. M. & Alaminos, E. Climate warming and activity period extension in the Mediterranean snake Malpolon monspessulanus. Clim. Change 92, 235–242 (2009).ADS 
Article 

Google Scholar 
9.Brown, G. P. & Shine, R. Effects of nest temperature and moisture on phenotypic traits of hatchling snakes (Tropidonophis mairii, Colubridae) from tropical Australia. Biol. J. Linn. Soc. 89, 159–168 (2006).Article 

Google Scholar 
10.Lourenço-de-Moraes, R. et al. Climate change will decrease the range size of snake species under negligible protection in the Brazilian Atlantic Forest hotspot. Sci. Rep. 9, 1–14 (2019).Article 
CAS 

Google Scholar 
11.Uetz, P., Freed, P. & Hošek, J. The Reptile Database. http://www.reptile-database.org (2019).12.Wallach, V., Wüster, W. & Broadley, D. G. In praise of subgenera: Taxonomic status of cobras of the genus. Zootaxa 2236, 26–36 (2009).Article 

Google Scholar 
13.Wüster, W. Taxonomic changes and toxinology: Systematic revisions of the Asiatic cobras (Naja naja species complex). Toxicon 34, 399–406 (1996).PubMed 
Article 

Google Scholar 
14.Wüster, W., Thorpe, R. S., Cox, M., Jintakune, P. & Nabhitabhata, J. Population systematics of the snake genus Naja (Reptilia: Serpentes: Elapidae) in Indochina: Multivariate morphometrics and comparative mitochondrial DNA sequencing (cytochrome oxidase I). J. Evol. Biol. 8, 493–510 (1995).Article 

Google Scholar 
15.Smith, M. A. The Fauna of British India Vol. 3 (Taylor and Francis, 1943).
Google Scholar 
16.Wüster, W. & Thorpe, R. S. Asiatic Cobras: Population systematics of the Naja naja Species Complex (Serpentes: Elapidae) in India and Central Asia. Herpetologica 48, 69–85 (1992).
Google Scholar 
17.IUCN. The IUCN Red List of Threatened Species. Version 2019-3. https://www.iucnredlist.org (2019).18.Tittensor, D. P. et al. A mid-term analysis of progress toward international biodiversity targets. Science 346, 241–243 (2014).ADS 
CAS 
Article 

Google Scholar 
19.Vitousek, P. M., Mooney, H. A., Lubchenco, J. & Melillo, J. M. Human domination of Earth’s ecosystems. Science 277, 494–499 (1997).CAS 
Article 

Google Scholar 
20.United Nations. World Population Prospects 2019. Department of Economic and Social Affairs. World Population Prospects 2019. (2019).21.UNESCAP. Factsheet: Urbanization trends in Asia and the Pacific 4 (2013).22.Zhou, Z. & Jiang, Z. International trade status and crisis for snake species in China. Conserv. Biol. 18, 1386–1394 (2004).Article 

Google Scholar 
23.Li, Y. & Li, D. The dynamics of trade in live wildlife across the Guangxi border between China and Vietnam during 1993–1996 and its control strategies. Biodivers. Conserv. 7, 895–914 (1998).Article 

Google Scholar 
24.CITES. CITES Appendices I, II, and III. (2019).25.Gutiérrez, J. M., Williams, D., Fan, H. W. & Warrell, D. A. Snakebite envenoming from a global perspective: Towards an integrated approach. Toxicon 56, 1223–1235 (2010).PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
26.Kasturiratne, A. et al. The global burden of snakebite: A literature analysis and modelling based on regional estimates of envenoming and deaths. PLoS Med. 5, 1591–1604 (2008).Article 

Google Scholar 
27.Longbottom, J. et al. Vulnerability to snakebite envenoming: A global mapping of hotspots. Lancet 392, 673–684 (2018).PubMed 
PubMed Central 
Article 

Google Scholar 
28.Warrell, D. A. Clinical toxicology of snakebite in Asia. In Handbook of Clinical Toxicology of Animal Venoms and Poisons (eds Meier, J. & White, J.) 493–594 (CRC Press, 1995).
Google Scholar 
29.Seto, K. C., Güneralp, B. & Hutyra, L. R. Global forecasts of urban expansion to 2030 and direct impacts on biodiversity and carbon pools. Proc. Natl. Acad. Sci. USA 109, 16083–16088 (2012).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
30.Yue, S., BoneBrake, T. C. & GiBSon, L. Human-snake conflict patterns in a dense urban-forest mosaic landscape. Herpetol. Conserv. Biol. 14, 143–154 (2019).
Google Scholar 
31.Yousefi, M., Kafash, A., Khani, A. & Nabati, N. Applying species distribution models in public health research by predicting snakebite risk using venomous snakes’ habitat suitability as an indicating factor. Sci. Rep. 10, 1–11 (2020).Article 
CAS 

Google Scholar 
32.Slowinski, J. B. & Wüster, W. A New Cobra (Elapidae: Naja) from Myanmar (Burma). Herpetologica 56, 257–270 (2000).
Google Scholar 
33.Wüster, W. & Thorpe, R. S. Population affinities of the asiatic cobra (Naja naja) species complex in south-east Asia: Reliability and random resampling. Biol. J. Linn. Soc. 36, 391–409 (1989).Article 

Google Scholar 
34.Wüster, W., Warrell, D. A., Cox, M. J., Jintakune, P. & Nabhitabhata, J. Redescription of Naja siamensis (Serpentes: Elapidae), a widely overlooked spitting cobra from S.E. Asia: Geographic variation, medical importance and designation of a neotype. J. Zool. 243, 771–788 (1997).Article 

Google Scholar 
35.Kuch, U. et al. A new species of krait (Squamata: Elapidae) from the Red River System of Northern Vietnam. Copeia 2005, 818–833 (2005).Article 

Google Scholar 
36.Journé, V., Barnagaud, J. Y., Bernard, C., Crochet, P. A. & Morin, X. Correlative climatic niche models predict real and virtual species distributions equally well. Ecology 101, 1–14 (2020).Article 

Google Scholar 
37.Kelly, M. Adaptation to climate change through genetic accommodation and assimilation of plastic phenotypes. Philos. Trans. R. Soc. B 374, 20180176 (2019).Article 

Google Scholar 
38.Siqueira, L. H. C. & Marques, O. A. V. Effects of Urbanization on Bothrops jararaca Populations in São Paulo Municipality, Southeastern Brazil. J. Herpetol. 52, 299–306 (2018).Article 

Google Scholar 
39.Santra, V. et al. Confirmation of Naja oxiana in Himachal Pradesh, India. Herpetol. Bull. https://doi.org/10.33256/hb150.2628 (2019).Article 

Google Scholar 
40.IUCN Standards and Petitions Committee. Guidelines for Using the IUCN Red List Categories and Criteria, Vol. 1 (2019).41.IUCN. Guidelines for Application of IUCN Red List Criteria At Regional And National Levels. (IUCN, 2012).42.Colwell, R. K., Brehm, G., Cardelús, C. L., Gilman, A. C. & Longino, J. T. Global warming, elevational range shifts, and lowland biotic attrition in the wet tropics. Science 322, 258–261 (2008).ADS 
CAS 
Article 

Google Scholar 
43.Sahlean, T. C., Gherghel, I., Papeş, M., Strugariu, A. & Zamfirescu, ŞR. Refining climate change projections for organisms with low dispersal abilities: A case study of the Caspian whip snake. PLoS ONE 9, e91994 (2014).ADS 
PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
44.Wolfe, A. K., Fleming, P. A. & Bateman, P. W. Impacts of translocation on a large urban-adapted venomous snake. Wildl. Res. 45, 316–324 (2018).Article 

Google Scholar 
45.Visser, M. E. Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc. R. Soc. B Biol. Sci. 275, 649–659 (2008).Article 

Google Scholar 
46.Chen, C., Qu, Y., Zhou, X. & Wang, Y. Human overexploitation and extinction risk correlates of Chinese snakes. Ecography (Cop.) 42, 1777–1788 (2019).Article 

Google Scholar 
47.CITES. Full CITES Trade Database 2000–2018. https://trade.cites.org/ (2018).48.Braimoh, A. K., Subramanian, S. M., Elliot, W. & Gasparatos, A. Climate and Human-Related Drivers of Biodiversity Decline in Southeast Asia. (United Nations University Institute of Advanced Studies, 2010) https://unu.edu/publications/articles/unraveling-the-drivers-of-southeast-asia-biodiversity-loss.html#info.49.Wood, S., Sebastian, K. & Scherr, S. Pilot Analysis of Global Ecosystems: Agroecosystems: A Joint Study (International Food Policy Research Institute and World Resources Institute, 2000).
Google Scholar 
50.Castelletta, M., Sodhi, N. S. & Subaraj, R. Heavy extinctions of forest avifauna in Singapore: Lessons for biodiversity conservation in Southeast Asia. Conserv. Biol. 14, 1870–1880 (2000).Article 

Google Scholar 
51.Zhao, S. et al. Land use change in Asia and the ecological consequences. Ecol. Res. 21, 890–896 (2006).Article 

Google Scholar 
52.Estoque, R. C. & Murayama, Y. Trends and spatial patterns of urbanization in Asia and Africa: A comparative analysis. In Urban Development in Asia and Africa 393–414 (2017).53.Shankar, P. G., Singh, A., Ganesh, S. R. & Whitaker, R. Factors influencing human hostility to King Cobras (Ophiophagus hannah) in the Western Ghats of India. Hamadryad 36, 91–100 (2013).
Google Scholar 
54.United Nations. Progress Towards the Sustainable Development Goals. https://undocs.org/en/E/2020/57 (2020).55.Nori, J., Carrasco, P. A. & Leynaud, G. C. Venomous snakes and climate change: Ophidism as a dynamic problem. Clim. Change 122, 67–80 (2014).ADS 
Article 

Google Scholar 
56.Organization, W. H. Snakebite Envenoming: A Strategy for Prevention and Control (World Health Organization, 2019).
Google Scholar 
57.Zancolli, G. et al. When one phenotype is not enough: Divergent evolutionary trajectories govern venom variation in a widespread rattlesnake species. Proc. R. Soc. B Biol. Sci. 286, 20182735 (2019).CAS 
Article 

Google Scholar 
58.Wüster, W. & Thorpe, R. S. Systematics and biogeography of the Asiatic cobra (Naja naja) species complex in the Philippine Islands. In Vertebrates in the Tropics (eds Peters, G. & Hutterer, R.) 333–344 (Museum Alexander Koenig, 1990).
Google Scholar 
59.Kazemi, E., Kaboli, M., Khosravi, R. & Khorasani, N. Evaluating the importance of environmental variables on spatial distribution of caspian cobra naja oxiana (Eichwald, 1831) in Iran. Asian Herpetol. Res. 10, 129–138 (2019).
Google Scholar 
60.Khan, M. The snakebite problem in Pakistan. Bull. Chicago Herp. Soc 49, 165–167 (2014).
Google Scholar 
61.Showler, D. A. A Checklist of the Amphibians and Reptiles of the Republic of Uzbekistan with a Review and Summary of Species Distribution. https://www.sustainablehoubaramanagement.org/wp-content/uploads/2018/09/Uzbekistan-Amphibian-Reptile-Checklist-14Sept2018-PDF.pdf (2018).62.Prakash, S., Kumar Mishra, A. & Raziuddin, M. A new record of cream coloured morph of Naja kaouthia Lesson, 1831 (Reptilia, Serpentes, Elapidae) from Hazaribag, Jharkhand, India. Biodivers. J. 3, 153–155 (2012).
Google Scholar 
63.Kazemi, E., Nazarizadeh, M., Fatemizadeh, F., Khani, A. & Kaboli, M. The phylogeny, phylogeography, and diversification history of the westernmost Asian cobra (Serpentes: Elapidae: Naja oxiana) in the Trans-Caspian region. Ecol. Evol. https://doi.org/10.1002/ece3.7144 (2020).Article 
PubMed 
PubMed Central 

Google Scholar 
64.Bivand, R. et al. Tools for Handling Spatial Objects. (2019).65.Lima-Ribeiro, M. et al. The ecoClimate Database. http://ecoclimate.org.66.Rangel, T. F. & Loyola, R. D. Labeling ecological niche models. Nat. Conserv. 10, 119–126 (2012).Article 

Google Scholar 
67.Beaumont, L. J., Hughes, L. & Poulsen, M. Predicting species distributions: Use of climatic parameters in BIOCLIM and its impact on predictions of species’ current and future distributions. Ecol. Model. 186, 251–270 (2005).Article 

Google Scholar 
68.Hijmans, R. J. et al. Geographic Data Analysis and Modeling. https://cran.r-project.org/package=raster (2019).69.Bivand, R. et al. Bindings for the ‘Geospatial’ Data Abstraction Library Version. Cran (2019).70.Pebesma, E. et al. Classes and Methods for Spatial Data. (R News, 2019).71.Hijmans, R. J., Phillips, S., Leathwick, J. & Elith, J. Species Distribution Modeling. (2017).72.Sharma, S. K. et al. Venomous Snakes of Nepal. (2013).73.Whitaker, R. & Captain, A. Snakes of India: The Field Guide. Draco Books (Chennai), (2008).74.Gao, J. Downscaling Global Spatial Population Projections from 1/8-degree to 1-km Grid Cells. NCAR Technical Note NCAR/TN-537+STR https://sedac.ciesin.columbia.edu/data/set/popdynamics-pop-projection-ssp-downscaled-1km-2010-2100. https://doi.org/10.5065/D60Z721H (2017).75.van Vuuren, D. P. et al. A new scenario framework for Climate Change Research: Scenario matrix architecture. Clim. Change 122, 373–386 (2014).Article 

Google Scholar  More

1.Falconer, D. S. & Mackay, T. F. C. Introduction to Quantitative Genetics, 4th edn (Longman, 1996).2.Xiong, W. et al. Nat. Plants https://doi.org/10.1038/s41477-021-00988-w (2021).3.Tadesse, W. et al. Crop Breed Genet Genom. 1, e190005 (2019).
Google Scholar 
4.Li, X., Guo, T., Mu, Q., Li, X. & Yu, J. Proc. Natl Acad. Sci. USA 115, 6679–6684 (2018).CAS 
Article 

Google Scholar 
5.Anderson, D. R. Model Based Inference in the Life Sciences (Springer, 2008).6.Zhao, Y. et al. Sci. Adv. 7, eabf9106 (2021).CAS 
Article 

Google Scholar 
7.Shi, L., Li, B., Kim, C., Kellnhofer, P. & Matusik, W. Nature 591, 234–239 (2021).CAS 
Article 

Google Scholar 
8.Li, J. et al. Mol. Ecol. 28, 3544–3560 (2019).CAS 
Article 

Google Scholar 
9.CGIAR. One CGIAR, https://www.cgiar.org/food-security-impact/one-cgiar/ More

1.Campbell, J. E. et al. Large historical growth in global terrestrial gross primary production. Nature 544, 84–87 (2017).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
2.Schwalm, C. R. et al. Modeling suggests fossil fuel emissions have been driving increased land carbon uptake since the turn of the 20th Century. Sci. Rep. 10, 9059 (2020).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
3.Wenzel, S., Cox, P. M., Eyring, V. & Friedlingstein, P. Projected land photosynthesis constrained by changes in the seasonal cycle of atmospheric CO2. Nature 538, 499–501 (2016).ADS 
PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
4.Piao, S. et al. Characteristics, drivers and feedbacks of global greening. Nat. Rev. Earth Environ. 1, 14–27 (2020).ADS 
Article 

Google Scholar 
5.Ellsworth, D. S. et al. Elevated CO2 does not increase eucalypt forest productivity on a low-phosphorus soil. Nat. Clim. Change 7, 279–282 (2017).ADS 
CAS 
Article 

Google Scholar 
6.Hararuk, O., Campbell, E. M., Antos, J. A. & Parish, R. Tree rings provide no evidence of a CO2 fertilization effect in old-growth subalpine forests of western Canada. Glob. Change Biol. 25, 1222–1234 (2019).ADS 
Article 

Google Scholar 
7.Jiang, M. et al. The fate of carbon in a mature forest under carbon dioxide enrichment. Nature 580, 227–231 (2020).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
8.Friedlingstein, P. et al. Uncertainties in CMIP5 climate projections due to carbon cycle feedbacks. J. Clim. 27, 511–526 (2014).ADS 
Article 

Google Scholar 
9.Koven, C. D. et al. Controls on terrestrial carbon feedbacks by productivity versus turnover in the CMIP5 earth system models. Biogeosciences 12, 5211–5228 (2015).ADS 
Article 

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

Google Scholar 
11.Sigurdsson, B. D., Medhurst, J. L., Wallin, G., Eggertsson, O. & Linder, S. Growth of mature boreal Norway spruce was not affected by elevated [CO2] and/or air temperature unless nutrient availability was improved. Tree Physiol. 33, 1192–1205 (2013).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
12.Walker, A. P. et al. Integrating the evidence for a terrestrial carbon sink caused by increasing atmospheric CO2. N. Phytol. 229, 2413–2445 (2021).CAS 
Article 

Google Scholar 
13.Gedalof, Z. & Berg, A. A. Tree ring evidence for limited direct CO2 fertilization of forests over the 20th century. Glob. Biogeochem. Cycles 24, (2010).14.van der Sleen, P. et al. No growth stimulation of tropical trees by 150 years of CO2 fertilization but water-use efficiency increased. Nat. Geosci. 8, 24–28 (2015).ADS 
Article 
CAS 

Google Scholar 
15.Girardin, M. P. et al. No growth stimulation of Canada’s boreal forest under half-century of combined warming and CO2 fertilization. Proc. Natl Acad. Sci. USA 113, E8406–E8414 (2016).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
16.Giguère-Croteau, C. et al. North America’s oldest boreal trees are more efficient water users due to increased [CO2], but do not grow faster. Proc. Natl Acad. Sci. USA 116, 2749–2754 (2019).ADS 
PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
17.Walker, A. P. et al. Decadal biomass increment in early secondary succession woody ecosystems is increased by CO2 enrichment. Nat. Commun. 10, 454 (2019).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
18.Du, E. et al. Global patterns of terrestrial nitrogen and phosphorus limitation. Nat. Geosci. https://doi.org/10.1038/s41561-019-0530-4 (2020).19.Schimel, J. P. & Bennett, J. Nitrogen mineralization: challenges of a changing paradigm. Ecology 85, 591–602 (2004).Article 

Google Scholar 
20.Vitousek, P. M. & Howarth, R. W. Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13, 87–115 (1991).Article 

Google Scholar 
21.Taylor, K. E., Stouffer, R. J. & Meehl, G. A. An overview of CMIP5 and the experiment design. Bull. Am. Meteorol. Soc. 93, 485–498 (2012).ADS 
Article 

Google Scholar 
22.Näsholm, T., Kielland, K. & Ganeteg, U. Uptake of organic nitrogen by plants. N. Phytol. 182, 31–48 (2009).Article 
CAS 

Google Scholar 
23.Lindahl, B. D. & Tunlid, A. Ectomycorrhizal fungi – potential organic matter decomposers, yet not saprotrophs. N. Phytol. 205, 1443–1447 (2015).CAS 
Article 

Google Scholar 
24.Terrer, C., Vicca, S., Hungate, B. A., Phillips, R. P. & Prentice, I. C. Mycorrhizal association as a primary control of the CO2 fertilization effect. Science 353, 72–74 (2016).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
25.Terrer, C. et al. Ecosystem responses to elevated CO2 governed by plant–soil interactions and the cost of nitrogen acquisition. N. Phytol. 217, 507–522 (2018).CAS 
Article 

Google Scholar 
26.Sulman, B. N. et al. Diverse Mycorrhizal associations enhance terrestrial C storage in a global model. Glob. Biogeochem. Cycles 33, 501–523 (2019).ADS 
CAS 
Article 

Google Scholar 
27.Terrer, C. et al. A trade-off between plant and soil carbon storage under elevated CO2. Nature 591, 599–603 (2021).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
28.Wieder, W. R., Cleveland, C. C., Smith, W. K. & Todd-Brown, K. Future productivity and carbon storage limited by terrestrial nutrient availability. Nat. Geosci. 8, 441–444 (2015).ADS 
CAS 
Article 

Google Scholar 
29.Smith, S. E. & Read, D. J. Mycorrhizal symbiosis. (Academic Press, 2010).30.Pellitier, P. T. & Zak, D. R. Ectomycorrhizal fungi and the enzymatic liberation of nitrogen from soil organic matter: why evolutionary history matters. N. Phytol. 217, 68–73 (2018).CAS 
Article 

Google Scholar 
31.Phillips, R. P. et al. Roots and fungi accelerate carbon and nitrogen cycling in forests exposed to elevated CO2. Ecol. Lett. 15, 1042–1049 (2012).PubMed 
Article 
PubMed Central 

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

Google Scholar 
33.Christian, N. & Bever, J. D. Carbon allocation and competition maintain variation in plant root mutualisms. Ecol. Evol. 8, 5792–5800 (2018).PubMed 
PubMed Central 
Article 

Google Scholar 
34.Hortal, S. et al. Role of plant–fungal nutrient trading and host control in determining the competitive success of ectomycorrhizal fungi. ISME J. 11, 2666–2676 (2017).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
35.Bogar, L. et al. Plant-mediated partner discrimination in ectomycorrhizal mutualisms. Mycorrhiza 29, 97–111 (2019).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
36.Bödeker, I. T. M., Nygren, C. M. R., Taylor, A. F. S., Olson, Å. & Lindahl, B. D. ClassII peroxidase-encoding genes are present in a phylogenetically wide range of ectomycorrhizal fungi. ISME J. 3, 1387–1395 (2009).PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
37.Hobbie, E. A. & Agerer, R. Nitrogen isotopes in ectomycorrhizal sporocarps correspond to belowground exploration types. Plant Soil 327, 71–83 (2010).CAS 
Article 

Google Scholar 
38.Koide, R. T., Fernandez, C. & Malcolm, G. Determining place and process: functional traits of ectomycorrhizal fungi that affect both community structure and ecosystem function. N. Phytol. 201, 433–439 (2014).Article 

Google Scholar 
39.Lindahl, B. D. et al. A group of ectomycorrhizal fungi restricts organic matter accumulation in boreal forest. Ecol. Lett. 24, 1341–1351 (2021).PubMed 
Article 
PubMed Central 

Google Scholar 
40.van der Linde, S. et al. Environment and host as large-scale controls of ectomycorrhizal fungi. Nature 558, 243–248 (2018).ADS 
PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
41.Read, D. J. & Perez-Moreno, J. Mycorrhizas and nutrient cycling in ecosystems: a journey towards relevance? N. Phytol. 157, 475–492 (2003).CAS 
Article 

Google Scholar 
42.Bödeker, I. T. M. et al. Ectomycorrhizal Cortinarius species participate in enzymatic oxidation of humus in northern forest ecosystems. N. Phytol. 203, 245–256 (2014).Article 
CAS 

Google Scholar 
43.Bogar, L. & Peay, K. Processes maintaining the coexistence of ectomycorrhizal fungi at a fine spatial scale. in Biogeography of Mycorrhizal Symbiosis (ed. Tedersoo, L.) vol. 230 79–105 (Springer, 2017).44.Xu, K. et al. Tree-ring widths are good proxies of annual variation in forest productivity in temperate forests. Sci. Rep. 7, 1945 (2017).ADS 
PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
45.Nehrbass‐Ahles, C. et al. The influence of sampling design on tree-ring-based quantification of forest growth. Glob. Change Biol. 20, 2867–2885 (2014).ADS 
Article 

Google Scholar 
46.Mathias, J. M. & Thomas, R. B. Disentangling the effects of acidic air pollution, atmospheric CO2, and climate change on recent growth of red spruce trees in the Central Appalachian Mountains. Glob. Change Biol. 24, 3938–3953 (2018).ADS 
Article 

Google Scholar 
47.Fierer, N., Barberán, A. & Laughlin, D. C. Seeing the forest for the genes: using metagenomics to infer the aggregated traits of microbial communities. Front. Microbiol. 5, 614 (2014).48.Zak, D. R. & Pregitzer, K. S. Spatial and temporal variability of nitrogen cycling in northern lower Michigan. Science 36, 367–380 (1990).
Google Scholar 
49.Zak, D. R., Pregitzer, K. S. & Host, G. E. Landscape variation in nitrogen mineralization and nitrification. Can. J. Res. 16, 1258–1263 (1986).Article 

Google Scholar 
50.Chen, J. & Gupta, A. K. Parametric Statistical Change Point Analysis: With Applications to Genetics, Medicine, and Finance. (Springer Science & Business Media, 2011).51.Thomas, R. Q., Canham, C. D., Weathers, K. C. & Goodale, C. L. Increased tree carbon storage in response to nitrogen deposition in the US. Nat. Geosci. 3, 13–17 (2010).ADS 
Article 
CAS 

Google Scholar 
52.Pellitier, P. T., Zak, D. R., Argiroff, W. A. & Upchurch, R. A. Coupled shifts in ectomycorrhizal communities and plant uptake of organic nitrogen along a soil gradient: an isotopic perspective. Ecosystems (2021).53.Sterkenburg, E., Clemmensen, K. E., Ekblad, A., Finlay, R. D. & Lindahl, B. D. Contrasting effects of ectomycorrhizal fungi on early and late stage decomposition in a boreal forest. ISME J. 12, 2187–2197 (2018).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
54.Lilleskov, E. A., Hobbie, E. A. & Fahey, T. J. Ectomycorrhizal fungal taxa differing in response to nitrogen deposition also differ in pure culture organic nitrogen use and natural abundance of nitrogen isotopes. N. Phytol. 154, 219–231 (2002).CAS 
Article 

Google Scholar 
55.Kohler, A. et al. Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat. Genet. 47, 410–415 (2015).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
56.Moeller, H. V., Peay, K. G. & Fukami, T. Ectomycorrhizal fungal traits reflect environmental conditions along a coastal California edaphic gradient. FEMS Microbiol. Ecol. 87, 797–806 (2014).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
57.Defrenne, C. E. et al. Shifts in Ectomycorrhizal fungal communities and exploration types relate to the environment and fine-root traits across interior douglas-fir forests of Western Canada. Front. Plant Sci. 10, 643 (2019).PubMed 
PubMed Central 
Article 

Google Scholar 
58.Fawal, N. et al. PeroxiBase: a database for large-scale evolutionary analysis of peroxidases. Nucleic Acids Res. 41, D441–D444 (2013).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
59.Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P. M. & Henrissat, B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42, D490–D495 (2014).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
60.Garajova, S. et al. Single-domain flavoenzymes trigger lytic polysaccharide monooxygenases for oxidative degradation of cellulose. Sci. Rep. 6, 28276 (2016).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
61.Janusz, G. et al. Lignin degradation: microorganisms, enzymes involved, genomes analysis and evolution. FEMS Microbiol. Rev. 41, 941–962 (2017).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
62.Shah, F. et al. Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors. N. Phytol. 209, 1705–1719 (2016).CAS 
Article 

Google Scholar 
63.Baldrian, P. Fungal laccases – occurrence and properties. FEMS Microbiol. Rev. 30, 215–242 (2006).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
64.Fernandez, C. W. & Kennedy, P. G. Revisiting the ‘Gadgil effect’: do interguild fungal interactions control carbon cycling in forest soils? N. Phytol. 209, 1382–1394 (2016).CAS 
Article 

Google Scholar 
65.Reich, P. B. et al. Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature 440, 922–925 (2006).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
66.Oren, R. et al. Soil fertility limits carbon sequestration by forest ecosystems in a CO2-enriched atmosphere. Nature 411, 469–472 (2001).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
67.Norby, R. J., Warren, J. M., Iversen, C. M., Medlyn, B. E. & McMurtrie, R. E. CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proc. Natl Acad. Sci. USA 107, 19368–19373 (2010).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
68.Andrew, C. & Lilleskov, E. A. Productivity and community structure of ectomycorrhizal fungal sporocarps under increased atmospheric CO2 and O3. Ecol. Lett. 12, 813–822 (2009).PubMed 
Article 
PubMed Central 

Google Scholar 
69.Näsholm, T. et al. Are ectomycorrhizal fungi alleviating or aggravating nitrogen limitation of tree growth in boreal forests? N. Phytol. 198, 214–221 (2013).Article 
CAS 

Google Scholar 
70.Finzi, A. C. et al. Increases in nitrogen uptake rather than nitrogen-use efficiency support higher rates of temperate forest productivity under elevated CO2. Proc. Natl Acad. Sci. USA 104, 14014–14019 (2007).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
71.Merkel, D. Soil Nutrients in Glaciated Michigan Landscapes: Distribution of Nutrients and Relationships with Stand Productivity. (Doctoral Thesis Submitted to Michigan State University, 1988).72.Host, G. E. & Pregitzer, K. S. Geomorphic influences on ground-flora and overstory composition in upland forests of northwestern lower Michigan. Can. J. Res. 22, 1547–1555 (1992).Article 

Google Scholar 
73.Edwards, I. P. & Zak, D. R. Phylogenetic similarity and structure of Agaricomycotina communities across a forested landscape. Mol. Ecol. 19, 1469–1482 (2010).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
74.Schimel, D., Stephens, B. B. & Fisher, J. B. Effect of increasing CO2 on the terrestrial carbon cycle. Proc. Natl Acad. Sci. USA 112, 436–441 (2015).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
75.Medlyn, B. E. et al. Using ecosystem experiments to improve vegetation models. Nat. Clim. Change 5, 528–534 (2015).ADS 
Article 

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

Google Scholar 
77.McClaugherty, C. A., Pastor, J., Aber, J. D. & Melillo, J. M. Forest litter decomposition in relation to soil nitrogen dynamics and litter quality. Ecology 66, 266–275 (1985).Article 

Google Scholar 
78.Pastor, J., Aber, J. D., McClaugherty, C. A. & Melillo, J. M. Aboveground production and N and P cycling along a nitrogen mineralization gradient on Blackhawk Island, Wisconsin. Ecology 65, 256–268 (1984).CAS 
Article 

Google Scholar 
79.Serra-Maluquer, X., Mencuccini, M. & Martínez-Vilalta, J. Changes in tree resistance, recovery and resilience across three successive extreme droughts in the northeast Iberian Peninsula. Oecologia 187, 343–354 (2018).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
80.Vitousek, P. Nutrient cycling and nutrient use efficiency. Am. Nat. 119, 553–572 (1982).Article 

Google Scholar 
81.Darrouzet-Nardi, A., Ladd, M. P. & Weintraub, M. N. Fluorescent microplate analysis of amino acids and other primary amines in soils. Soil Biol. Biochem. 57, 78–82 (2013).CAS 
Article 

Google Scholar 
82.Ibáñez, I., Zak, D. R., Burton, A. J. & Pregitzer, K. S. Anthropogenic nitrogen deposition ameliorates the decline in tree growth caused by a drier climate. Ecology 99, 411–420 (2018).PubMed 
Article 
PubMed Central 

Google Scholar 
83.Lines, E. R., Zavala, M. A., Purves, D. W. & Coomes, D. A. Predictable changes in aboveground allometry of trees along gradients of temperature, aridity and competition. Glob. Ecol. Biogeogr. 21, 1017–1028 (2012).Article 

Google Scholar 
84.Taylor, D. L. et al. Accurate estimation of fungal diversity and abundance through improved lineage-specific primers optimized for illumina amplicon sequencing. Appl. Environ. Microbiol. 82, 7217–7226 (2016).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
85.Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
86.Nilsson, R. H. et al. The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res. 47, D259–D264 (2019).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
87.Konar, A. et al. High-quality genetic mapping with ddRADseq in the non-model tree Quercus rubra. BMC Genomics 18, 417 (2017).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
88.Sork, V. L. et al. First draft assembly and annotation of the genome of a California Endemic oak. Genes|Genomes|Genet. 6, 3485–3495 (2016).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
89.Wood, D. E., Lu, J. & Langmead, B. Improved metagenomic analysis with Kraken 2. Genome Biol. 20, 257 (2019).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
90.Buchfink, B., Xie, C. & Huson, D. H. Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12, 59–60 (2015).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
91.Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
92.Treiber, M. L., Taft, D. H., Korf, I., Mills, D. A. & Lemay, D. G. Pre- and post-sequencing recommendations for functional annotation of human fecal metagenomes. BMC Bioinforma. 21, 74 (2020).CAS 
Article 

Google Scholar 
93.Peng, M. et al. Comparative analysis of basidiomycete transcriptomes reveals a core set of expressed genes encoding plant biomass degrading enzymes. Fungal Genet. Biol. 112, 40–46 (2018).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
94.Floudas, D. et al. Uncovering the hidden diversity of litter-decomposition mechanisms in mushroom-forming fungi. ISME J. https://doi.org/10.1038/s41396-020-0667-6 (2020).95.Kriventseva, E. V. et al. OrthoDB v10: sampling the diversity of animal, plant, fungal, protist, bacterial and viral genomes for evolutionary and functional annotations of orthologs. Nucleic Acids Res. 47, D807–D811 (2019).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
96.Quinn, T. P., Erb, I., Richardson, M. F. & Crowley, T. M. Understanding sequencing data as compositions: an outlook and review. Bioinformatics 34, 2870–2878 (2018).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
97.Ferrier, S., Manion, G., Elith, J. & Richardson, K. Using generalized dissimilarity modelling to analyse and predict patterns of beta diversity in regional biodiversity assessment. Divers. Distrib. 13, 252–264 (2007).Article 

Google Scholar 
98.Duhamel, M. et al. Plant selection initiates alternative successional trajectories in the soil microbial community after disturbance. Ecol. Monogr. 89, e01367 (2019).Article 

Google Scholar 
99.Qin, C., Zhu, K., Chiariello, N. R., Field, C. B. & Peay, K. G. Fire history and plant community composition outweigh decadal multi-factor global change as drivers of microbial composition in an annual grassland. J. Ecol. 108, 611–625 (2020).CAS 
Article 

Google Scholar 
100.Oksanen, J., et al. Package vegan.101.Wickham, H. et al. Welcome to the Tidyverse. J. Open Source Softw. 4, 1686 (2019).ADS 
Article 

Google Scholar 
102.Spiegelhalter, D. J., Best, N. G., Carlin, B. P. & Linde, A. V. D. Bayesian measures of model complexity and fit. J. R. Stat. Soc. Ser. B Stat. Methodol. 64, 583–639 (2002).MathSciNet 
MATH 
Article 

Google Scholar  More

.readcube-buybox { display: none !important;}

After cyclones in the north Atlantic, droves of emaciated, dead seabirds can wash ashore on North American and European beaches. New research probes the cause of these mass-mortality events, called winter wrecks, and suggests that climate change might worsen the pattern1.

Access options

Access through your institution

Change institution

Buy or subscribe

/* style specs start */
style{display:none!important}.LiveAreaSection-193358632 *{align-content:stretch;align-items:stretch;align-self:auto;animation-delay:0s;animation-direction:normal;animation-duration:0s;animation-fill-mode:none;animation-iteration-count:1;animation-name:none;animation-play-state:running;animation-timing-function:ease;azimuth:center;backface-visibility:visible;background-attachment:scroll;background-blend-mode:normal;background-clip:borderBox;background-color:transparent;background-image:none;background-origin:paddingBox;background-position:0 0;background-repeat:repeat;background-size:auto auto;block-size:auto;border-block-end-color:currentcolor;border-block-end-style:none;border-block-end-width:medium;border-block-start-color:currentcolor;border-block-start-style:none;border-block-start-width:medium;border-bottom-color:currentcolor;border-bottom-left-radius:0;border-bottom-right-radius:0;border-bottom-style:none;border-bottom-width:medium;border-collapse:separate;border-image-outset:0s;border-image-repeat:stretch;border-image-slice:100%;border-image-source:none;border-image-width:1;border-inline-end-color:currentcolor;border-inline-end-style:none;border-inline-end-width:medium;border-inline-start-color:currentcolor;border-inline-start-style:none;border-inline-start-width:medium;border-left-color:currentcolor;border-left-style:none;border-left-width:medium;border-right-color:currentcolor;border-right-style:none;border-right-width:medium;border-spacing:0;border-top-color:currentcolor;border-top-left-radius:0;border-top-right-radius:0;border-top-style:none;border-top-width:medium;bottom:auto;box-decoration-break:slice;box-shadow:none;box-sizing:border-box;break-after:auto;break-before:auto;break-inside:auto;caption-side:top;caret-color:auto;clear:none;clip:auto;clip-path:none;color:initial;column-count:auto;column-fill:balance;column-gap:normal;column-rule-color:currentcolor;column-rule-style:none;column-rule-width:medium;column-span:none;column-width:auto;content:normal;counter-increment:none;counter-reset:none;cursor:auto;display:inline;empty-cells:show;filter:none;flex-basis:auto;flex-direction:row;flex-grow:0;flex-shrink:1;flex-wrap:nowrap;float:none;font-family:initial;font-feature-settings:normal;font-kerning:auto;font-language-override:normal;font-size:medium;font-size-adjust:none;font-stretch:normal;font-style:normal;font-synthesis:weight style;font-variant:normal;font-variant-alternates:normal;font-variant-caps:normal;font-variant-east-asian:normal;font-variant-ligatures:normal;font-variant-numeric:normal;font-variant-position:normal;font-weight:400;grid-auto-columns:auto;grid-auto-flow:row;grid-auto-rows:auto;grid-column-end:auto;grid-column-gap:0;grid-column-start:auto;grid-row-end:auto;grid-row-gap:0;grid-row-start:auto;grid-template-areas:none;grid-template-columns:none;grid-template-rows:none;height:auto;hyphens:manual;image-orientation:0deg;image-rendering:auto;image-resolution:1dppx;ime-mode:auto;inline-size:auto;isolation:auto;justify-content:flexStart;left:auto;letter-spacing:normal;line-break:auto;line-height:normal;list-style-image:none;list-style-position:outside;list-style-type:disc;margin-block-end:0;margin-block-start:0;margin-bottom:0;margin-inline-end:0;margin-inline-start:0;margin-left:0;margin-right:0;margin-top:0;mask-clip:borderBox;mask-composite:add;mask-image:none;mask-mode:matchSource;mask-origin:borderBox;mask-position:0% 0%;mask-repeat:repeat;mask-size:auto;mask-type:luminance;max-height:none;max-width:none;min-block-size:0;min-height:0;min-inline-size:0;min-width:0;mix-blend-mode:normal;object-fit:fill;object-position:50% 50%;offset-block-end:auto;offset-block-start:auto;offset-inline-end:auto;offset-inline-start:auto;opacity:1;order:0;orphans:2;outline-color:initial;outline-offset:0;outline-style:none;outline-width:medium;overflow:visible;overflow-wrap:normal;overflow-x:visible;overflow-y:visible;padding-block-end:0;padding-block-start:0;padding-bottom:0;padding-inline-end:0;padding-inline-start:0;padding-left:0;padding-right:0;padding-top:0;page-break-after:auto;page-break-before:auto;page-break-inside:auto;perspective:none;perspective-origin:50% 50%;pointer-events:auto;position:static;quotes:initial;resize:none;right:auto;ruby-align:spaceAround;ruby-merge:separate;ruby-position:over;scroll-behavior:auto;scroll-snap-coordinate:none;scroll-snap-destination:0 0;scroll-snap-points-x:none;scroll-snap-points-y:none;scroll-snap-type:none;shape-image-threshold:0;shape-margin:0;shape-outside:none;tab-size:8;table-layout:auto;text-align:initial;text-align-last:auto;text-combine-upright:none;text-decoration-color:currentcolor;text-decoration-line:none;text-decoration-style:solid;text-emphasis-color:currentcolor;text-emphasis-position:over right;text-emphasis-style:none;text-indent:0;text-justify:auto;text-orientation:mixed;text-overflow:clip;text-rendering:auto;text-shadow:none;text-transform:none;text-underline-position:auto;top:auto;touch-action:auto;transform:none;transform-box:borderBox;transform-origin:50% 50% 0;transform-style:flat;transition-delay:0s;transition-duration:0s;transition-property:all;transition-timing-function:ease;vertical-align:baseline;visibility:visible;white-space:normal;widows:2;width:auto;will-change:auto;word-break:normal;word-spacing:normal;word-wrap:normal;writing-mode:horizontalTb;z-index:auto;-webkit-appearance:none;-moz-appearance:none;-ms-appearance:none;appearance:none;margin:0}.LiveAreaSection-193358632{width:100%}.LiveAreaSection-193358632 .login-option-buybox{display:block;width:100%;font-size:17px;line-height:30px;color:#222;padding-top:30px;font-family:Harding,Palatino,serif}.LiveAreaSection-193358632 .additional-access-options{display:block;font-weight:700;font-size:17px;line-height:30px;color:#222;font-family:Harding,Palatino,serif}.LiveAreaSection-193358632 .additional-login >li:not(:first-child)::before{transform:translateY(-50%);content:”;height:1rem;position:absolute;top:50%;left:0;border-left:2px solid #999}.LiveAreaSection-193358632 .additional-login >li:not(:first-child){padding-left:10px}.LiveAreaSection-193358632 .additional-login >li{display:inline-block;position:relative;vertical-align:middle;padding-right:10px}.BuyBoxSection-683559780{display:flex;flex-wrap:wrap;flex:1;flex-direction:row-reverse;margin:-30px -15px 0}.BuyBoxSection-683559780 .box-inner{width:100%;height:100%}.BuyBoxSection-683559780 .readcube-buybox{background-color:#f3f3f3;flex-shrink:1;flex-grow:1;flex-basis:255px;background-clip:content-box;padding:0 15px;margin-top:30px}.BuyBoxSection-683559780 .subscribe-buybox{background-color:#f3f3f3;flex-shrink:1;flex-grow:4;flex-basis:300px;background-clip:content-box;padding:0 15px;margin-top:30px}.BuyBoxSection-683559780 .title-readcube{display:block;margin:0;margin-right:20%;margin-left:20%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .title-buybox{display:block;margin:0;margin-right:29%;margin-left:29%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .title-asia-buybox{display:block;margin:0;margin-right:5%;margin-left:5%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .asia-link{color:#069;cursor:pointer;text-decoration:none;font-size:1.05em;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:1.05em6}.BuyBoxSection-683559780 .access-readcube{display:block;margin:0;margin-right:10%;margin-left:10%;font-size:14px;color:#222;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .access-asia-buybox{display:block;margin:0;margin-right:5%;margin-left:5%;font-size:14px;color:#222;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .access-buybox{display:block;margin:0;margin-right:30%;margin-left:30%;font-size:14px;color:#222;opacity:.8px;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .price-buybox{display:block;font-size:30px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;padding-top:30px;text-align:center}.BuyBoxSection-683559780 .price-from{font-size:14px;padding-right:10px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .issue-buybox{display:block;font-size:13px;text-align:center;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:19px}.BuyBoxSection-683559780 .no-price-buybox{display:block;font-size:13px;line-height:18px;text-align:center;padding-right:10%;padding-left:10%;padding-bottom:20px;padding-top:30px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif}.BuyBoxSection-683559780 .vat-buybox{display:block;margin-top:5px;margin-right:20%;margin-left:20%;font-size:11px;color:#222;padding-top:10px;padding-bottom:15px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:17px}.BuyBoxSection-683559780 .button-container{display:block;padding-right:20px;padding-left:20px}.BuyBoxSection-683559780 .button-container >a:hover,.Button-505204839:hover,.Button-1078489254:hover{text-decoration:none}.BuyBoxSection-683559780 .readcube-button{background:#fff;margin-top:30px}.BuyBoxSection-683559780 .button-asia{background:#069;border:1px solid #069;border-radius:0;cursor:pointer;display:block;padding:9px;outline:0;text-align:center;text-decoration:none;min-width:80px;margin-top:75px}.BuyBoxSection-683559780 .button-label-asia,.ButtonLabel-3869432492,.ButtonLabel-3296148077{display:block;color:#fff;font-size:17px;line-height:20px;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;text-align:center;text-decoration:none;cursor:pointer}.Button-505204839,.Button-1078489254{background:#069;border:1px solid #069;border-radius:0;cursor:pointer;display:block;padding:9px;outline:0;text-align:center;text-decoration:none;min-width:80px;margin-top:10px}.Button-505204839 .readcube-label,.Button-1078489254 .readcube-label{color:#069}
/* style specs end */Subscribe to JournalGet full journal access for 1 year$199.00only $3.90 per issueSubscribeAll prices are NET prices. VAT will be added later in the checkout.Tax calculation will be finalised during checkout.Rent or Buy articleGet time limited or full article access on ReadCube.from$8.99Rent or BuyAll prices are NET prices.

Additional access options:

Log in

Learn about institutional subscriptions

doi: https://doi.org/10.1038/d41586-021-02494-7

References1.Clairbaux, M. et al. Curr. Biol. https://doi.org/10.1016/j.cub.2021.06.059 (2021)Article 

Google Scholar 
Download references

Subjects

Ecology

Latest on:

Ecology

Preventing spillover as a key strategy against pandemics
Correspondence 14 SEP 21

Pollination advantage of rare plants unveiled
News & Views 08 SEP 21

Pollinators contribute to the maintenance of flowering plant diversity
Article 08 SEP 21

Jobs

Postdoctoral fellow

Dalhousie University
Halifax, Canada

Postdoctoral Research Fellowship in Pharmacogenomics and Clinical Pharmacology with a Focus on Adverse Drug Reactions

The University of British Columbia (UBC)
Vancouver, Canada

English Speaking Secretary for the Institute Director

Jülich Research Centre (FZJ)
Aachen, Germany

Officer for Strategic Support of Research Grant Applications

German Cancer Research Center in the Helmholtz Association (DKFZ)
Heidelberg, Germany More