Philippa Kaur

Plant materials and genome sequencingFresh leaves of a wild P. koreana plant in the Changbai Mountains of Jilin province in China were collected, and the total genomic DNA was extracted using the CTAB method. For the Illumina short-read sequencing, paired-end libraries with insert sizes of 350 bp were constructed and sequenced using an Illumina HiSeq X Ten platform. For the long-read sequencing, the genomic libraries with 20-kbp insertions were constructed and sequenced using the PromethION platform of Oxford Nanopore Technologies (ONT). For the Hi-C experiment, approximately 3 g of fresh young leaves of the same P. koreana accession was ground to powder in liquid nitrogen. A sequencing library was then constructed by chromatin extraction and digestion, DNA ligation, purification, and fragmentation53 and was subsequently sequenced on an Illumina HiSeq X Ten platform.Genome assembly and scaffoldingThe quality-controlled reads were first corrected via a self-align method using the NextCorrect module in the software NextDenovo v2.0-beta.1 (https://github.com/Nextomics/NextDenovo) with parameters “reads_cutoff=1k (filter reads with length 20, percent of unqualified bases More

Loarie, S. R. et al. The velocity of climate change. Nature 462, 1052–1055 (2009).Article 
ADS 
PubMed 

Google Scholar 
Yoshida, T., Jones, L. E., Ellner, S. P., Fussmann, G. F. & Hairston, N. G. Rapid evolution drives ecological dynamics in a predator–prey system. Nature 424, 303–306 (2003).Article 
ADS 
PubMed 

Google Scholar 
terHorst, C. P., Miller, T. E. & Levitan, D. R. Evolution of prey in ecological time reduces the effect size of predators in experimental microcosms. Ecology 91, 629–636 (2010).Article 
PubMed 

Google Scholar 
Duffy, M. A. & Sivars-Becker, L. Rapid evolution and ecological host-parasite dynamics. Ecol. Lett. 10, 44–53 (2007).Article 
PubMed 

Google Scholar 
Diamond, S. E., Chick, L. D., Perez, A., Strickler, S. A. & Martin, R. A. Evolution of thermal tolerance and its fitness consequences: parallel and non-parallel responses to urban heat islands across three cities. Proc. Biol. Sci. 285, 20180036 (2018).PubMed 
PubMed Central 

Google Scholar 
Franks, S. J., Sim, S. & Weis, A. E. Rapid evolution of flowering time by an annual plant in response to a climate fluctuation. Proc. Natl. Acad. Sci. USA 104, 1278–1282 (2007).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
terHorst, C. P., Lennon, J. T. & Lau, J. A. The relative importance of rapid evolution for plant-microbe interactions depends on ecological context. Proc. R. Soc. B Biol. Sci. 281, 20140028 (2014).Article 

Google Scholar 
Bradshaw, W. E. & Holzapfel, C. M. Evolutionary response to rapid climate change. Science https://doi.org/10.1126/science.1127000 (2006).Article 
PubMed 

Google Scholar 
Gonzalez, A., Ronce, O., Ferriere, R. & Hochberg, M. E. Evolutionary rescue: an emerging focus at the intersection between ecology and evolution. Philos. Trans. R. Soc. B Biol. Sci. 368, 20120404 (2013).Article 

Google Scholar 
Carlson, S. M., Cunningham, C. J. & Westley, P. A. H. Evolutionary rescue in a changing world. Trends Ecol. Evol. 29, 521–530 (2014).Article 
PubMed 

Google Scholar 
Lau, J. A. & terHorst, C. P. Evolutionary responses to global change in species-rich communities. Ann. N. Y. Acad. Sci. 1476, 43–58 (2020).Article 
ADS 
PubMed 

Google Scholar 
Lau, J. A., Shaw, R. G., Reich, P. B. & Tiffin, P. Indirect effects drive evolutionary responses to global change. New Phytol. 201, 335–343 (2014).Article 
PubMed 

Google Scholar 
Tseng, M. & O’Connor, M. I. Predators modify the evolutionary response of prey to temperature change. Biol. Lett. 11, 20150798 (2015).Article 
PubMed 
PubMed Central 

Google Scholar 
terHorst, C. P. et al. Evolution in a community context: Trait responses to multiple species interactions. Am. Nat. 191, 368–380 (2018).Article 

Google Scholar 
Hussa, E. A. & Goodrich-Blair, H. It takes a village: Ecological and fitness impacts of multipartite mutualism. Annu. Rev. Microbiol. 67, 161–178 (2013).Article 
PubMed 

Google Scholar 
Hoegh-Guldberg, O. Climate change, coral bleaching and the future of the world’s coral reefs. Mar. Freshw. Res. 50, 839–866 (1999).
Google Scholar 
Death, G., Fabricius, K. E., Sweatman, H. & Puotinen, M. The 27–year decline of coral cover on the Great Barrier Reef and its causes. PNAS 109, 17995–17999 (2012).Article 
ADS 

Google Scholar 
Heron, S. F., Maynard, J. A., van Hooidonk, R. & Eakin, C. M. Warming trends and bleaching stress of the world’s coral reefs 1985–2012. Sci. Rep. 6, 38402 (2016).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
van Hooidonk, R. et al. Local-scale projections of coral reef futures and implications of the Paris Agreement. Sci Rep 6, 39666 (2016).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
Oliver, J. K., Berkelmans, R. & Eakin, C. M. Coral bleaching in space and time. In Coral Bleaching: Patterns, Processes, Causes and Consequences (eds. van Oppen, M. J. H. & Lough, J. M.) 27–49 (Springer, 2018). https://doi.org/10.1007/978-3-540-69775-6_3.Hughes, T. P. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80–83 (2018).Article 
ADS 
PubMed 

Google Scholar 
Impacts of 1.5°C global warming on natural and human systems. In Global Warming of 1.5°C: IPCC Special Report on Impacts of Global Warming of 1.5°C above Pre-industrial Levels in Context of Strengthening Response to Climate Change, Sustainable Development, and Efforts to Eradicate Poverty (ed. IPCC) 175–312 (Cambridge University Press, 2022). https://doi.org/10.1017/9781009157940.005.Glynn, P. W. & D’Croz, L. Experimental evidence for high temperature stress as the cause of El Niño-coincident coral mortality. Coral Reefs 8, 181–191 (1990).Article 
ADS 

Google Scholar 
Eakin, C. M. et al. Caribbean corals in crisis: Record thermal stress, bleaching, and mortality in 2005. PLoS ONE 5, e13969 (2010).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
Eakin, C. M., Sweatman, H. P. A. & Brainard, R. E. The 2014–2017 global-scale coral bleaching event: insights and impacts. Coral Reefs 38, 539–545 (2019).Article 
ADS 

Google Scholar 
Baker, A. C., Starger, C. J., McClanahan, T. R. & Glynn, P. W. Corals’ adaptive response to climate change. Nature 430, 741–741 (2004).Article 
ADS 
PubMed 

Google Scholar 
Mieog, J. C., Van Oppen, M. J. H., Berkelmans, R., Stam, W. T. & Olsen, J. L. Quantification of algal endosymbionts (Symbiodinium) in coral tissue using real-time PCR. Mol. Ecol. Resour. 9, 74–82 (2009).Article 
PubMed 

Google Scholar 
Silverstein, R. N., Correa, A. M. S. & Baker, A. C. Specificity is rarely absolute in coral–algal symbiosis: Implications for coral response to climate change. Proc. R. Soc. B Biol. Sci. 279, 2609–2618 (2012).Article 

Google Scholar 
Hoadley, K. D. et al. Host–symbiont combinations dictate the photo-physiological response of reef-building corals to thermal stress. Sci. Rep. 9, 9985 (2019).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
Parkinson, J. E. & Baums, I. B. The extended phenotypes of marine symbioses: ecological and evolutionary consequences of intraspecific genetic diversity in coral-algal associations. Front. Microbiol. 5, 445 (2014).Article 
PubMed 
PubMed Central 

Google Scholar 
Karim, W., Nakaema, S. & Hidaka, M. Temperature effects on the growth rates and photosynthetic activities of symbiodinium cells. J. Mar. Sci. Eng. 3, 368–381 (2015).Article 

Google Scholar 
Grégoire, V., Schmacka, F., Coffroth, M. A. & Karsten, U. Photophysiological and thermal tolerance of various genotypes of the coral endosymbiont Symbiodinium sp. (Dinophyceae). J. Appl. Phycol. 29, 1893 (2017).Article 

Google Scholar 
Díaz-Almeyda, E. M. et al. Intraspecific and interspecific variation in thermotolerance and photoacclimation in Symbiodinium dinoflagellates. Proc. R. Soc. B Biol. Sci. 284, 20171767 (2017).Article 

Google Scholar 
Bayliss, S. L. J., Scott, Z. R., Coffroth, M. A. & terHorst, C. P. Genetic variation in Breviolum antillogorgium, a coral reef symbiont, in response to temperature and nutrients. Ecol. Evol. 9, 2803–2813 (2019).Article 
PubMed 
PubMed Central 

Google Scholar 
Pelosi, J., Eaton, K. M., Mychajliw, S., terHorst, C. P. & Coffroth, M. A. Thermally tolerant symbionts may explain Caribbean octocoral resilience to heat stress. Coral Reefs 40, 1113–1125 (2021).Article 

Google Scholar 
Zilber-Rosenberg, I. & Rosenberg, E. Role of microorganisms in the evolution of animals and plants: The hologenome theory of evolution. Fems Microbiol. Rev. 32, 723–735 (2008).Article 
PubMed 

Google Scholar 
Howells, E. J. et al. Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat. Clim. Chang. 2, 116–120 (2012).Article 
ADS 

Google Scholar 
Chakravarti, L. J., Beltran, V. H. & van Oppen, M. J. H. Rapid thermal adaptation in photosymbionts of reef-building corals. Glob. Chang. Biol. 23, 4675–4688 (2017).Article 
ADS 
PubMed 

Google Scholar 
Chakravarti, L. J. & van Oppen, M. J. H. Experimental evolution in coral photosymbionts as a tool to increase thermal tolerance. Front. Mar. Sci. 5, 227 (2018).Article 

Google Scholar 
Buerger, P. et al. Heat-evolved microalgal symbionts increase coral bleaching tolerance. Sci. Adv. https://doi.org/10.1126/sciadv.aba2498 (2020).Article 
PubMed 
PubMed Central 

Google Scholar 
Hofmann, D. K. & Kremer, B. P. Carbon metabolism and strobilation in Cassiopea andromedea (Cnidaria: Scyphozoa): Significance of endosymbiotic dinoflagellates. Mar. Boil. 65, 25 (1981).Article 

Google Scholar 
Welsh, D., Dunn, R. & Meziane, T. Oxygen and nutrient dynamics of the upside down jellyfish (Cassiopea sp.) and its influence on benthic nutrient exchanges and primary production. Hydrobiologia 635, 351 (2009).Article 

Google Scholar 
Freeman, C. J., Stoner, E. W., Easson, C. G., Matterson, K. O. & Baker, D. M. Symbiont carbon and nitrogen assimilation in the Cassiopea-Symbiodinium mutualism. Mar. Ecol. Prog. Ser. https://doi.org/10.3354/meps11605 (2016).Article 

Google Scholar 
Bigelow, R. P. The Anatomy and Development of Cassiopea xamachana. 1–72 (Pub. by the Boston Society of Natural History, 1900). https://doi.org/10.5962/bhl.title.31420.Colley, N. J. & Trench, R. K. Selectivity in phagocytosis and persistence of symbiotic algae in the scyphistoma stage of the jellyfish Cassiopeia xamachana. Proc. R. Soc. Lond. B Biol. Sci. 219, 61–82 (1983).Article 
ADS 
PubMed 

Google Scholar 
Hofmann, D. K., Fitt, W. K. & Fleck, J. Checkpoints in the life-cycle of Cassiopea spp.: Control of metagenesis and metamorphosis in a tropical jellyfish. Int. J. Dev. Biol. 40, 331–338 (1996).PubMed 

Google Scholar 
Stat, M. & Gates, R. D. Clade D symbiodinium in scleractinian corals: A “Nugget” of hope, a selfish opportunist, an ominous sign, or all of the above?. J. Mar. Biol. 2011, e730715 (2010).
Google Scholar 
Correa, A. M. S. & Baker, A. C. Disaster taxa in microbially mediated metazoans: how endosymbionts and environmental catastrophes influence the adaptive capacity of reef corals. Glob. Change Biol. 17, 68–75 (2011).Article 
ADS 

Google Scholar 
Silverstein, R. N., Cunning, R. & Baker, A. C. Change in algal symbiont communities after bleaching, not prior heat exposure, increases heat tolerance of reef corals. Glob. Chang. Biol. 21, 236–249 (2015).Article 
ADS 
PubMed 

Google Scholar 
Leal, M. C. et al. Symbiont type influences trophic plasticity of a model cnidarian-dinoflagellate symbiosis. J. Exp. Biol. 218, 858–863 (2015).Article 
PubMed 

Google Scholar 
Klein, S. G. et al. Symbiodinium mitigate the combined effects of hypoxia and acidification on a noncalcifying cnidarian. Glob. Chang. Biol. 23, 3690–3703 (2017).Article 
ADS 
PubMed 

Google Scholar 
Cziesielski, M. J. et al. Multi-omics analysis of thermal stress response in a zooxanthellate cnidarian reveals the importance of associating with thermotolerant symbionts. Proc. R. Soc. B. 285, 20172654 (2018).Article 
PubMed 
PubMed Central 

Google Scholar 
Cunning, R. & Baker, A. C. Thermotolerant coral symbionts modulate heat stress-responsive genes in their hosts. Mol. Ecol. 29, 2940–2950 (2020).Article 
PubMed 

Google Scholar 
Newkirk, C. R., Frazer, T. K., Martindale, M. Q. & Schnitzler, C. E. Adaptation to bleaching: Are thermotolerant symbiodiniaceae strains more successful than other strains under elevated temperatures in a model symbiotic cnidarian?. Front. Microbiol. 11, 822 (2020).Article 
PubMed 
PubMed Central 

Google Scholar 
Trench, R. K. MICROALGAL-INVERTEBRATESYMBIOSES: A REVIEW. Cell Res. 41 (1993).Yellowlees, D., Rees, T. A. V. & Leggat, W. Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ. 31, 679–694 (2008).Article 
PubMed 

Google Scholar 
Swain, T. D., Chandler, J., Backman, V. & Marcelino, L. Consensus thermotolerance ranking for 110 Symbiodinium phylotypes: an exemplar utilization of a novel iterative partial-rank aggregation tool with broad application potential. Funct. Ecol. 31, 172–183 (2017).Article 

Google Scholar 
Klueter, A., Trapani, J., Archer, F. I., McIlroy, S. E. & Coffroth, M. A. Comparative growth rates of cultured marine dinoflagellates in the genus Symbiodinium and the effects of temperature and light. PLoS ONE 12, e0187707 (2017).Article 
PubMed 
PubMed Central 

Google Scholar 
Chen, B. et al. Dispersal, genetic variation, and symbiont interaction network of heat-tolerant endosymbiont Durusdinium trenchii: Insights into the adaptive potential of coral to climate change. Sci. Total Environ. 723, 138026 (2020).Article 
ADS 
PubMed 

Google Scholar 
van Oppen, M. J. H., Souter, P., Howells, E. J., Heyward, A. & Berkelmans, R. Novel genetic diversity through somatic mutations: Fuel for adaptation of reef corals?. Diversity 3, 405–423 (2011).Article 

Google Scholar 
van Oppen, M. J. H., Oliver, J. K., Putnam, H. M. & Gates, R. D. Building coral reef resilience through assisted evolution. Proc. Natl. Acad. Sci. USA 112, 2307–2313 (2015).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
Ohdera, A. H. et al. Upside-down but headed in the right direction: Review of the highly versatile Cassiopea xamachana system. Front. Ecol. Evol. 6, 35 (2018).Article 

Google Scholar 
Fitt, W. K. & Costley, K. The role of temperature in survival of the polyp stage of the tropical rhizostome jellyfish Cassiopea xamachana. J. Exp. Mar. Biol. Ecol. 222, 79–91 (1998).Article 

Google Scholar 
Aljbour, S. M., Zimmer, M. & Kunzmann, A. Cellular respiration, oxygen consumption, and trade-offs of the jellyfish Cassiopea sp. in response to temperature change. Journal of Sea Research 128, 92–97 (2017).Rahat, M. & Adar, O. Effect of symbiotic zooxanthellae and temperature on budding and strobiliation in Cassiopeia andromeda (Eschscholz). Biol. Bull. 159, 394–401 (1980).Article 

Google Scholar 
Cole, L. C. The population consequences of life history phenomena. Q. Rev. Biol. 29, 103–137 (1954).Article 
PubMed 

Google Scholar 
Brommer, J. E., Merilä, J. & Kokko, H. Reproductive timing and individual fitness. Ecol. Lett. 5, 802–810 (2002).Article 

Google Scholar 
Hofmann, D. K., Neumann, R. & Henne, K. Strobilation, budding and initiation of scyphistoma morphogenesis in the rhizostome Cassiopea andromeda (Cnidaria: Scyphozoa). Mar. Biol. 47, 161–176 (1978).Article 

Google Scholar 
Thornhill, D. J., LaJeunesse, T. C., Kemp, D. W., Fitt, W. K. & Schmidt, G. W. Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar. Biol. 148, 711–722 (2006).Article 

Google Scholar 
Mellas, R. E., McIlroy, S. E., Fitt, W. K. & Coffroth, M. A. Variation in symbiont uptake in the early ontogeny of the upside-down jellyfish, Cassiopea spp.. J. Exp. Mar. Biol. Ecol. 459, 38–44 (2014).Article 

Google Scholar 
Fransolet, D., Roberty, S. & Plumier, J.-C. Establishment of endosymbiosis: The case of cnidarians and Symbiodinium. J. Exp. Mar. Biol. Ecol. 420–421, 1–7 (2012).Article 

Google Scholar 
Jones, A. M., Berkelmans, R., van Oppen, M. J. H., Mieog, J. C. & Sinclair, W. A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc. R. Soc. B Biol. Sci. 275, 1359–1365 (2008).Article 

Google Scholar 
Baskett, M. L., Gaines, S. D. & Nisbet, R. M. Symbiont diversity may help coral reefs survive moderate climate change. Ecol. Appl. 19, 3–17 (2009).Article 
PubMed 

Google Scholar 
Baker, A. C. Reef corals bleach to survive change. Nature 411, 765–766 (2001).Article 
ADS 
PubMed 

Google Scholar 
Berkelmans, R. & van Oppen, M. J. H. The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proc. R. Soc. B Biol. Sci. 273, 2305–2312 (2006).Article 

Google Scholar 
Davy, S. K., Allemand, D. & Weis, V. M. Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol. Mol. Biol. Rev. 76, 229–261 (2012).Article 
PubMed 
PubMed Central 

Google Scholar 
Wolfowicz, I. et al. Aiptasia sp. larvae as a model to reveal mechanisms of symbiont selection in cnidarians. Sci. Rep. 6, 32366 (2016).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
Little, A. F., van Oppen, M. J. H. & Willis, B. L. Flexibility in algal endosymbioses shapes growth in reef corals. Science https://doi.org/10.1126/science.1095733 (2004).Article 
PubMed 

Google Scholar 
Jones, A. & Berkelmans, R. Potential costs of acclimatization to a warmer climate: Growth of a reef coral with heat tolerant vs sensitive symbiont types. PLOS ONE 5, e10437 (2010).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
Ortiz, J. C., González-Rivero, M. & Mumby, P. J. Can a thermally tolerant symbiont improve the future of Caribbean coral reefs?. Glob. Change Biol. 19, 273–281 (2013).Article 
ADS 

Google Scholar 
Sprouffske, K. & Wagner, A. Growthcurver: An R package for obtaining interpretable metrics from microbial growth curves. BMC Bioinform. 17, 172 (2016).Article 

Google Scholar  More

COVID variant family expandsSince the Omicron variant of SARS-CoV-2 emerged in late 2021, it has spawned a series of subvariants that have sparked global waves of infection. In the past few months, scientists have identified more than a dozen extra subvariants to watch. There are so many that they’re being called a swarm, or ‘variant soup’. BQ.1.1 (a descendant of BQ.1) and XBB seem to be rising to the top, possibly because they have many mutations in a key region of the viral spike protein called the receptor binding domain, which is required to infect cells.

Source: NextStrain

The variants near youIn Europe and North America, SARS-CoV-2 variants in the BQ.1 family are rising quickly and are likely to drive infection waves as these regions enter winter. They are also a common ingredient of the variant soup in South Africa, Nigeria and elsewhere in Africa. XBB, by contrast, looks likely to dominate infections in Asia; it recently drove a wave of infections in Singapore.

Source: Moritz Gerstung, Cov-Spectrum.org and GISAID

Money worries for science studentsEighty-five per cent of graduate students who responded to a Nature survey are worried about the increasing cost of living, and 25% are concerned about their growing student debt. Forty-five per cent said that rising inflation could cause them to reconsider whether to continue their science studies. The survey involved more than 3,200 self-selected PhD and master’s students from around the world.

How species suffer in heatwavesEven a small temperature rise has a severe effect on animal mortality, and understanding this relationship is important for predicting the effects of heatwaves caused by climate change. A paper in Nature used published data to examine how changes in temperature affect the rate of biological processes, such as movement or metabolism, at permissive temperatures — those at which species function normally. They also looked at how higher, stressful temperatures affect the rate of heat failure (irreversible heat injuries that result in death). This graph shows that rising temperatures drive a very rapid increase in heat-failure rates in frogs and molluscs. These high sensitivities suggest that when there is no way to escape hot conditions, species can quickly succumb. More

Duarte, C. M. et al. The soundscape of the Anthropocene ocean. Science 371, eaba4658 (2021).Article 
CAS 
PubMed 

Google Scholar 
Hylland, K. & Vethaak, A. D. Ecological Impacts of Toxic Chemicals (Bentham Science Publishers, 2012).Bossart, G. D. Marine mammals as sentinel species for oceans and human health. Vet. Pathol. 48, 676–690 (2011).Article 
CAS 
PubMed 

Google Scholar 
Worm, B., Lotze, H. K., Jubinville, I., Wilcox, C. & Jambeck, J. Plastic as a persistent marine pollutant. Annu. Rev. Environ. Resour. 42, 1–26 (2017).Article 

Google Scholar 
Borrelle, S. B. et al. Predicted growth in plastic waste exceeds efforts to mitigate plastic pollution. Science 369, 1515–1518 (2020).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Geyer, R., Jambeck, J. R. & Law, K. L. Production, use, and fate of all plastics ever made. Sci. Adv. 3, e1700782 (2017).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
Carpenter, E. J., Anderson, S. J., Harvey, G. R., Miklas, H. P. & Peck, B. B. Polystyrene spherules in coastal waters. Science 178, 749–750 (1972).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Kenyon, K. W. & Kridler, E. Laysan albatrosses swallow indigestible matter. Auk 86, 339–343 (1969).Article 

Google Scholar 
Santos, R. G., Machovsky-Capuska, G. E. & Andrades, R. Plastic ingestion as an evolutionary trap: toward a holistic understanding. Science 373, 56–60 (2021).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Suaria, G. et al. Microfibers in oceanic surface waters: a global characterization. Sci. Adv. 6, 1–9 (2020).Article 

Google Scholar 
Nelms, S. E., Galloway, T. S., Godley, B. J., Jarvis, D. S. & Lindeque, P. K. Investigating microplastic trophic transfer in marine top predators. Environ. Pollut. 238, 999–1007 (2018).Article 
CAS 
PubMed 

Google Scholar 
Bucci, K., Tulio, M. & Rochman, C. M. What is known and unknown about the effects of plastic pollution: a meta-analysis and systematic review. Ecol. Appl. 30, e02044 (2020).Article 
CAS 
PubMed 

Google Scholar 
Savoca, M. S., McInturf, A. G. & Hazen, E. L. Plastic ingestion by marine fish is widespread and increasing. Glob. Change Biol. 27, 2188–2199 (2021).Article 
ADS 
CAS 

Google Scholar 
Lynch, J. M. Quantities of marine debris ingested by sea turtles: Global meta-analysis highlights need for standardized data reporting methods and reveals relative risk. Environ. Sci. Technol. 52, 12026–12038 (2018).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Wilcox, C., Van Sebille, E. & Hardesty, B. D. Threat of plastic pollution to seabirds is global, pervasive, and increasing. Proc. Natl Acad. Sci. USA 112, 11899–11904 (2015).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Fossi, M. C. et al. Are baleen whales exposed to the threat of microplastics? A case study of the Mediterranean fin whale (Balaenoptera physalus). Mar. Pollut. Bull. 64, 2374–2379 (2012).Article 
CAS 
PubMed 

Google Scholar 
Germanov, E. S., Marshall, A. D., Bejder, L., Fossi, M. C. & Loneragan, N. R. Microplastics: no small problem for filter-feeding megafauna. Trends Ecol. Evol. 33, 227–232 (2018).Article 
PubMed 

Google Scholar 
Alava, J. J. Modeling the bioaccumulation and biomagnification potential of microplastics in a Cetacean foodweb of the Northeastern pacific: a prospective tool to assess the risk exposure to plastic particles. Front. Mar. Sci. 7, 566101 (2020).Article 

Google Scholar 
Zantis, L. J. et al. Assessing microplastic exposure of large marine filter-feeders. Sci. Total Environ. https://doi.org/10.1016/j.scitotenv.2021.151815. (2021).Garcia-Garin, O. et al. Ingestion of synthetic particles by fin whales feeding off Western Iceland in summer. Chemosphere 279, 130564 (2021).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Sims, D. W. & Quayle, V. A. Selective foraging behaviour of basking sharks on zooplankton in a small-scale front. Nature 393, 460–465 (1998).Article 
ADS 
CAS 

Google Scholar 
Goldbogen, J. A. et al. Prey density and distribution drive the three-dimensional foraging strategies of the largest filter feeder. Funct. Ecol. 29, 951–961 (2015).Article 

Google Scholar 
Frias, J. P. G. L., Otero, V. & Sobral, P. Evidence of microplastics in samples of zooplankton from Portuguese coastal waters. Mar. Environ. Res. 95, 89–95 (2014).Article 
CAS 
PubMed 

Google Scholar 
Sun, X., Liang, J., Zhu, M., Zhao, Y. & Zhang, B. Microplastics in seawater and zooplankton from the Yellow Sea*. Environ. Pollut. 242, 585–595 (2018).Article 
CAS 
PubMed 

Google Scholar 
Tanaka, K. & Takada, H. Microplastic fragments and microbeads in digestive tracts of planktivorous fish from urban coastal waters. Sci. Rep. 6, 34351 (2016).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Cole, M. et al. Microplastic ingestion by zooplankton. Environ. Sci. Technol. 47, 6646–6655 (2013).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Mahara, N. et al. Assessing size-based exposure to microplastic particles and ingestion pathways in zooplankton and herring in a coastal pelagic ecosystem of British Columbia, Canada. Mar. Ecol. Prog. Ser. 683, 139–155 (2022).Article 
ADS 
CAS 

Google Scholar 
Besseling, E. et al. Microplastic in a macro filter feeder: humpback whale Megaptera novaeangliae. Mar. Pollut. Bull. 95, 248–252 (2015).Article 
CAS 
PubMed 

Google Scholar 
Baini, M. et al. First detection of seven phthalate esters (PAEs) as plastic tracers in superficial neustonic/planktonic samples and cetacean blubber. Anal. Methods 9, 1512–1520 (2017).Article 
CAS 

Google Scholar 
Goldbogen, J. A. et al. How Baleen whales feed: the biomechanics of engulfment and filtration. Annu. Rev. Mar. Sci. 9, 367–386 (2017).Article 
ADS 
CAS 

Google Scholar 
Kawamura, A. A Review of Food of Balaenopterid Whales (AGRIS, 1980).Fleming, A. H., Clark, C. T., Calambokidis, J. & Barlow, J. Humpback whale diets respond to variance in ocean climate and ecosystem conditions in the California Current. Glob. Change Biol. 22, 1214–1224 (2015).Article 
ADS 

Google Scholar 
Clapham, P. J., Leatherwood, S., Szczepaniak, I. & Brownell, R. L. Catches of humpback and other whales from shore stations at Moss Landing and Trinidad, California, 1919–1926. Mar. Mammal. Sci. 13, 368–394 (1997).Article 

Google Scholar 
Savoca, M. S. et al. Baleen whale prey consumption based on high-resolution foraging measurements. Nature 599, 85–90 (2021).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Kahane-Rapport, S. R. & Goldbogen, J. A. Allometric scaling of morphology and engulfment capacity in rorqual whales. J. Morphol. 279, 1256–1268 (2018).Article 
PubMed 

Google Scholar 
Kahane-Rapport, S. R. et al. Lunge filter feeding biomechanics constrain rorqual foraging ecology across scale. J. Exp. Biol. 223, jeb224196 (2020).Goldbogen, J. A., Potvin, J. & Shadwick, R. E. Skull and buccal cavity allometry increase mass-specific engulfment capacity in fin whales. Proc. R. Soc. B: Biol. Sci. 277, 861–868 (2010).Article 

Google Scholar 
Cade, D. E., Carey, N., Domenici, P., Potvin, J. & Goldbogen, J. A. Predator-informed looming stimulus experiments reveal how large filter feeding whales capture highly maneuverable forage fish. Proc. Natl Acad. Sci. USA 117, 472–478 (2020).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Domenici, P. The scaling of locomotor performance in predator-prey encounters: from fish to killer whales. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 131, 169–182 (2001).Article 
CAS 
PubMed 

Google Scholar 
Lindstedt, S. & Caldor, W. Body size, physiological time, and longevity of homeothermic animals. Q. Rev. Biol. 56, 1–16 (1981).Article 

Google Scholar 
Banavar, J. R. et al. A general basis for quarter-power scaling in animals. Proc. Natl Acad. Sci. USA 107, 15816–15820 (2010).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Fossi, M. C. et al. Fin whales and microplastics: the Mediterranean Sea and the Sea of Cortez scenarios. Environ. Pollut. 209, 68–78 (2016).Article 
CAS 
PubMed 

Google Scholar 
Croll et al. Encyclopedia of Marine Mammals 2nd edn (Elsevier, 2018).De Vos, A., Pattiaratchi, C. B. & Harcourt, R. G. Inter-annual variability in blue whale distribution off Southern Sri Lanka between 2011 and 2012. J. Mar. Sci. Eng. 2, 534–550 (2014).Article 

Google Scholar 
Torres, L. G., Barlow, D. R., Chandler, T. E. & Burnett, J. D. Insight into the kinematics of blue whale surface foraging through drone observations and prey data. PeerJ 8, e8906 (2020).Article 
PubMed 
PubMed Central 

Google Scholar 
Friedlaender, A. S. et al. The advantages of diving deep: fin whales quadruple their energy intake when targeting deep krill patches. Funct. Ecol. https://doi.org/10.1111/1365-2435.13471 (2019).Kashiwabara, L. et al. Microplastics and microfibers in surface waters of Monterey Bay National Marine Sanctuary, California. Mar. Pollut. Bull. 165, 112148 (2021).Article 
CAS 
PubMed 

Google Scholar 
Lattin, G. L., Moore, C. J., Zellers, A. F., Moore, S. L. & Weisberg, S. B. A comparison of neustonic plastic and zooplankton at different depths near the southern California shore. Mar. Pollut. Bull. 49, 291–294 (2004).Article 
CAS 
PubMed 

Google Scholar 
Sutton, R. et al. Understanding Microplastic Levels, Pathways, and Transport in the San Francisco Bay Region. (2019).Choy, C. A. et al. The vertical distribution and biological transport of marine microplastics across the epipelagic and mesopelagic water column. Sci. Rep. 9, 7843 (2019).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
Desforges, J. P. W., Galbraith, M. & Ross, P. S. Ingestion of microplastics by zooplankton in the Northeast Pacific Ocean. Arch. Environ. Contamination Toxicol. 69, 320–330 (2015).Article 
CAS 

Google Scholar 
Rochman, C. M. et al. Anthropogenic debris in seafood: plastic debris and fibers from textiles in fish and bivalves sold for human consumption. Sci. Rep. 5, 14340 (2015).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Fossi, M. C., Baini, M. & Simmonds, M. P. Cetaceans as ocean health indicators of marine litter impact at global scale. Front. Environ. Sci. https://doi.org/10.3389/fenvs.2020.586627 (2020).Pabortsava, K. & Lampitt, R. S. High concentrations of plastic hidden beneath the surface of the Atlantic Ocean. Nat. Commun. 11, 4073 (2020).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Cong, Y. et al. Ingestion, egestion and post-exposure effects of polystyrene microspheres on marine medaka (Oryzias melastigma). Chemosphere 228, 93–100 (2019).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Ory, N. C., Gallardo, C., Lenz, M. & Thiel, M. Capture, swallowing, and egestion of microplastics by a planktivorous juvenile fish. Environ. Pollut. 240, 566–573 (2018).Article 
CAS 
PubMed 

Google Scholar 
Grigorakis, S., Mason, S. A. & Drouillard, K. G. Determination of the gut retention of plastic microbeads and microfibers in goldfish (Carassius auratus). Chemosphere 169, 233–238 (2017).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Gigault, J. et al. Current opinion: What is a nanoplastic? Environ. Pollut. 235, 1030–1034 (2018).Article 
CAS 
PubMed 

Google Scholar 
Lu, Y. et al. Uptake and accumulation of polystyrene microplastics in zebrafish (Danio rerio) and toxic effects in liver. Environ. Sci. Technol. 50, 4054–4060 (2016).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Barboza, L. G. A. et al. Microplastics in wild fish from North East Atlantic Ocean and its potential for causing neurotoxic effects, lipid oxidative damage, and human health risks associated with ingestion exposure. Sci. Total Environ. 717, 134625 (2020).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Ramsperger, A. F. R. M. et al. Environmental exposure enhances the internalization of microplastic particles into cells. Sci. Adv. 6, 1–10 (2020).Article 

Google Scholar 
Collard, F. et al. Microplastics in livers of European anchovies (Engraulis encrasicolus, L.). Environ. Pollut. 229, 1000–1005 (2017).Article 
CAS 
PubMed 

Google Scholar 
Dawson, A. L. et al. Turning microplastics into nanoplastics through digestive fragmentation by Antarctic krill. Nat. Commun. 9, 1001 (2018).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
Wieczorek, A. M. et al. Frequency of microplastics in mesopelagic fishes from the Northwest Atlantic. Front. Mar. Sci. 5, 1–9 (2018).
Google Scholar 
Boerger, C. M., Lattin, G. L., Moore, S. L. & Moore, C. J. Plastic ingestion by planktivorous fishes in the North Pacific Central Gyre. Mar. Pollut. Bull. 60, 2275–2278 (2010).Article 
CAS 
PubMed 

Google Scholar 
Davison, P. & Asch, R. Plastic ingestion by mesopelagic fishes in the North Pacific Subtropical Gyre. Mar. Ecol. Prog. Ser. 432, 173–180 (2011).Article 
ADS 

Google Scholar 
Lusher, A. L., Donnell, C. O., Officer, R. & Connor, I. O. Microplastic interactions with North Atlantic mesopelagic fish. ICES J. Mar. Sci. 73, 1214–1225 (2016).Article 

Google Scholar 
Hamilton, B. M. et al. Prevalence of microplastics and anthropogenic debris within a deep-sea food web. Mar. Ecol. Prog. Ser. 675, 23–33 (2021).Article 
ADS 

Google Scholar 
Sun, X. et al. Ingestion of microplastics by natural zooplankton groups in the northern. Mar. Pollut. Bull. 115, 217–224 (2017).Article 
CAS 
PubMed 

Google Scholar 
Mayo, C. A. & Marx, M. K. Surface foraging behaviour of the North Atlantic right whale, Eubalaena glacialis, and associated zooplankton characteristics. Can. J. Zool. 68, 2214–2220 (1990).Article 

Google Scholar 
Friedlaender, A. S. et al. Diel changes in humpback whale Megaptera novaeangliae feeding behavior in response to sand lance Ammodytes spp. behavior and distribution. Mar. Ecol. Prog. Ser. 395, 91–100 (2009).Article 
ADS 

Google Scholar 
Tekman, M. B. et al. Tying up loose ends of microplastic pollution in the arctic: distribution from the sea surface through the water column to deep-sea sediments at the HAUSGARTEN observatory. Environ. Sci. Technol. 54, 4079–4090 (2020).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Woodall, L. C. et al. The deep sea is a major sink for microplastic debris. R. Soc. Open Sci. 1, 140317 (2014).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
Iwata, T. et al. Tread-water feeding of Bryde’s whales. Curr. Biol. 27, R1154–R1155 (2017).Article 
CAS 
PubMed 

Google Scholar 
Gregorietti, M. et al. Cetacean presence and distribution in the central Mediterranean Sea and potential risks deriving from plastic pollution. Mar. Pollut. Bull. 173, 112943 (2021).Article 
CAS 
PubMed 

Google Scholar 
Rosel, P. E., Wilcox, L. A., Yamada, T. K. & Mullin, K. D. A new species of baleen whale (Balaenoptera) from the Gulf of Mexico, with a review of its geographic distribution. Marine Mammal Sci. https://doi.org/10.1111/mms.12776 (2021).Yong, M. M. H. et al. Microplastics in fecal samples of whale sharks (Rhincodon typus) and from surface water in the Philippines. Microplastics Nanoplastics 1, 17 (2021).Article 
PubMed 

Google Scholar 
Fossi, M. C. et al. Are whale sharks exposed to persistent organic pollutants and plastic pollution in the Gulf of California (Mexico)? First ecotoxicological investigation using skin biopsies. Comp. Biochem. Physiol. Part C: Toxicol. Pharmacol. 199, 48–58 (2017).CAS 

Google Scholar 
Cade, D. E. et al. Predator‐scale spatial analysis of intra‐patch prey distribution reveals the energetic drivers of rorqual whale super‐group formation. Funct. Ecol. 35, 894–908 (2021).Article 
CAS 

Google Scholar 
Goldbogen, J. A. et al. Why whales are big but not bigger: Physiological drivers and ecological limits in the age of ocean giants. Science 366, 1367–1372 (2019).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Southall, B. L. et al. Behavioral responses of individual blue whales (Balaenoptera musculus) to mid-frequency military sonar. J. Exp. Biol. 222, jeb190637 (2019).Article 
PubMed 

Google Scholar 
Calambokidis, J. et al. Differential vulnerability to ship strikes between day and night for blue, fin, and humpback whales based on dive and movement data from Medium duration archival tags. Front. Mar. Sci. 6, 543 (2019).Article 

Google Scholar 
Cade, D. E. et al. Tools for integrating inertial sensor data with video bio-loggers, including estimation of animal orientation, motion, and position. Anim. Biotelem. 9, 34 (2021).Article 

Google Scholar 
Cade, D. E., Friedlaender, A. S., Calambokidis, J. & Goldbogen, J. A. Kinematic diversity in rorqual whale feeding mechanisms. Curr. Biol. 26, 2617–2624 (2016).Article 
CAS 
PubMed 

Google Scholar 
Johnson, M. P. & Tyack, P. L. A digital acoustic recording tag for measuring the response of wild marine mammals to sound. IEEE J. Ocean. Eng. 28, 3–12 (2003).Article 
ADS 

Google Scholar 
Cade, D. E., Barr, K. R., Calambokidis, J., Friedlaender, A. S. & Goldbogen, J. A. Determining forward speed from accelerometer jiggle in aquatic environments. J. Exp. Biol. 221, jeb170449 (2018).PubMed 

Google Scholar 
Hadfield, J. MCMC methods for multi-response generalised linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010).Article 

Google Scholar 
Hipfner, J. M. et al. Two forage fishes as potential conduits for the vertical transfer of microfibres in Northeastern Pacific Ocean food webs. Environ. Pollut. 239, 215–222 (2018).Article 
CAS 
PubMed 

Google Scholar 
Doyle, M. J., Watson, W., Bowlin, N. M. & Sheavly, S. B. Plastic particles in coastal pelagic ecosystems of the Northeast Pacific ocean. Mar. Environ. Res. 71, 41–52 (2011).Article 
CAS 
PubMed 

Google Scholar 
Witteveen, B. H., Worthy, G. A. J., Foy, R. J. & Wynne, K. M. Modeling the diet of humpback whales: An approach using stable carbon and nitrogen isotopes in a Bayesian mixing model. Mar. Mammal. Sci. 28, E233–E250 (2012).Article 

Google Scholar  More

Woolhouse MEJ, Gowtage-Sequeria S. Host range and emerging and reemerging pathogens. Emerg Infect Dis. 2005;11:1842–7.Article 
PubMed 
PubMed Central 

Google Scholar 
Allen T, Murray KA, Zambrana-Torrelio C, Morse SS, Rondinini C, Di Marco M, et al. Global hotspots and correlates of emerging zoonotic diseases. Nat Commun. 2017;8:1–10.Article 
CAS 

Google Scholar 
Van Kerkhove MD, Ly S, Holl D, Guitian J, Mangtani P, Ghani AC, et al. Frequency and patterns of contact with domestic poultry and potential risk of H5N1 transmission to humans living in rural Cambodia. Influenza Other Respir Viruses. 2008;2:155–63.Article 
PubMed 
PubMed Central 

Google Scholar 
Gaythorpe KAM, Hamlet A, Cibrelus L, Garske T, Ferguson NM. The effect of climate change on yellow fever disease burden in Africa. eLife. 2020;9:1–27.Article 

Google Scholar 
Faust CL, McCallum HI, Bloomfield LSP, Gottdenker NL, Gillespie TR, Torney CJ, et al. Pathogen spillover during land conversion. Ecol Lett. 2018;21:471–83.Article 
PubMed 

Google Scholar 
Gog J, Woodroffe R, Swinton J. Disease in endangered metapopulations: The importance of alternative hosts. Proc R Soc B Biol Sci. 2002;269:671–6.Article 

Google Scholar 
Jones BA, Grace D, Kock R, Alonso S, Rushton J, Said MY, et al. Zoonosis emergence linked to agricultural intensification and environmental change. Proc Natl Acad Sci USA. 2013;110:8399–404.Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
White LA, Forester JD, Craft ME. Disease outbreak thresholds emerge from interactions between movement behavior, landscape structure, and epidemiology. Proc Natl Acad Sci USA. 2018;115:7374–9.Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Altizer S, Bartel R, Han BA. Animal migration and infectious disease risk. Science. 2011;331:296–302.Article 
CAS 
PubMed 

Google Scholar 
Ludwig SC, Roos S, Bubb D, Baines D. Long-term trends in abundance and breeding success of red grouse and hen harriers in relation to changing management of a Scottish grouse moor. Wildl Biol. 2017;2017:wlb.00246.Article 

Google Scholar 
Newton I. Weather-related mass-mortality events in migrants. Ibis. 2007;149:453–67.Article 

Google Scholar 
Ropert-Coudert Y, Kato A, Meyer X, Pellé M, MacIntosh AJJ, Angelier F, et al. A complete breeding failure in an Adélie penguin colony correlates with unusual and extreme environmental events. Ecography. 2015;38:111–3.Article 

Google Scholar 
Newmark WD, Stanley TR. Habitat fragmentation reduces nest survival in an Afrotropical bird community in a biodiversity hotspot. Proc Natl Acad Sci USA. 2011;108:11488–93.Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Tuyttens FaM, Macdonald DW, Rogers LM, Cheeseman CL, Roddam AW. Comparative study on the consequences of culling badgers (Meles meles) on biometrics, population dynamics and movement. J Anim Ecol. 2000;69:567–80.Article 

Google Scholar 
Frafjord K. Influence of reproductive status: Home range size in water voles (Arvicola amphibius). PLoS ONE. 2016;11:1–13.Article 

Google Scholar 
Begg CM, Begg KS, Du Toit JT, Mills MGL. Spatial organization of the honey badger Mellivora capensis in the southern Kalahari: Home-range size and movement patterns. J Zool. 2005;265:23–35.Article 

Google Scholar 
Bronikowski AM, Cords M, Alberts SC, Altmann J, Brockman DK, Fedigan LM, et al. Female and male life tables for seven wild primate species. Sci Data. 2016;3:1–8.Article 

Google Scholar 
Mitchell GW, Woodworth BK, Taylor PD, Norris DR. Automated telemetry reveals age specific differences in flight duration and speed are driven by wind conditions in a migratory songbird. Mov Ecol. 2015;3:1–13.Article 

Google Scholar 
Frankish CK, Manica A, Phillips RA. Effects of age on foraging behavior in two closely related albatross species. Mov Ecol. 2020;8:1–17.Article 

Google Scholar 
Tirpak JM, Giuliano WM, Allen TJ, Bittner S, Edwards JW, Friedhof S, et al. Ruffed grouse-habitat preference in the central and southern Appalachians. Ecol Manag. 2010;260:1525–38.Article 

Google Scholar 
Zhu WW, Garber PA, Bezanson M, Qi XG, Li BG. Age- and sex-based patterns of positional behavior and substrate utilization in the golden snub-nosed monkey (Rhinopithecus roxellana). Am J Primatol. 2015;77:98–108.Article 
PubMed 

Google Scholar 
Tian H, Yu P, Bjørnstad ON, Cazelles B, Yang J, Tan H, et al. Anthropogenically driven environmental changes shift the ecological dynamics of hemorrhagic fever with renal syndrome. PLOS Pathog. 2017;13:e1006198.Article 
PubMed 
PubMed Central 

Google Scholar 
George DB, Webb CT, Farnsworth ML, O’Shea TJ, Bowen RA, Smith DL, et al. Host and viral ecology determine bat rabies seasonality and maintenance. Proc Natl Acad Sci USA. 2011;108:10208–13.Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
van Dijk JG, Verhagen JH, Wille M, Waldenström J. Host and virus ecology as determinants of influenza A virus transmission in wild birds. Curr Opin Virol. 2018;28:26–36.Article 
PubMed 

Google Scholar 
Chong R, Shi M, Grueber CE, Holmes EC, Hogg CJ, Belov K, et al. Fecal Viral Diversity of Captive and Wild Tasmanian Devils Characterized Using Virion-Enriched Metagenomics and Metatranscriptomics. J Virol. 2019;93:e00205–19.Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
François S, Pybus OG. Towards an understanding of the avian virome. J Gen Virol. 2020;101:785–90.Article 
PubMed 
PubMed Central 

Google Scholar 
Springer A, Fichtel C, Al-Ghalith GA, Koch F, Amato KR, Clayton JB, et al. Patterns of seasonality and group membership characterize the gut microbiota in a longitudinal study of wild Verreaux’s sifakas (Propithecus verreauxi). Ecol Evol. 2017;7:5732–45.Article 
PubMed 
PubMed Central 

Google Scholar 
Aivelo T, Laakkonen J, Jernvall J. Population-and individual-level dynamics of the intestinal microbiota of a small primate. Appl Environ Microbiol. 2016;82:3537–45.Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
van Dongen WFD, White J, Brandl HB, Moodley Y, Merkling T, Leclaire S, et al. Age-related differences in the cloacal microbiota of a wild bird species. BMC Ecol. 2013;13:11.Cleaveland S, Laurenson MK, Taylor LH. Diseases of humans and their domestic mammals: Pathogen characteristics, host range and the risk of emergence. Philos Trans R Soc B Biol Sci. 2001;356:991–9.Article 
CAS 

Google Scholar 
Wille M, Shi M, Hurt AC, Klaassen M, Holmes EC. RNA virome abundance and diversity is associated with host age in a bird species. Virology. 2021;561:98–106.Article 
CAS 
PubMed 

Google Scholar 
Negrey JD, Thompson ME, Langergraber KE, Machanda ZP, Mitani JC, Muller MN, et al. Demography, life-history trade-offs, and the gastrointestinal virome of wild chimpanzees. Philos Trans R Soc B Biol Sci. 2020;375:20190613.Article 

Google Scholar 
Hill SC, Manvell RJ, Schulenburg B, Shell W, Wikramaratna PS, Perrins C, et al. Antibody responses to avian influenza viruses in wild birds broaden with age. Proc R Soc B Biol Sci. 2016;283:20162159.Article 

Google Scholar 
Perrins CM, Ogilvie MA. A study of the Abbotsbury mute swans (Cygnus olor). Wildfowl. 1981;32:35–47.
Google Scholar 
Perrins CM, McCleery RH, Ogilvie MA. A study of the breeding Mute Swans Cygnus olor at Abbotsbury. Wildfowl. 1994;45:1–14.
Google Scholar 
Perrins C. Survival rates of young mute swans Cygnus olor. Wildfowl Suppl. 1991;45:95–103.
Google Scholar 
McCleery RH, Perrins C, Wheeler D, Groves S. Population structure, survival rates and productivity of mute swans breeding in a colony at Abbotsbury, Dorset, England. Waterbirds Waterbird Soc. 2002;25:201.
Google Scholar 
Matrozis R A 30-year (1988–2017) study of Mute Swans Cygnus olor in Riga, Latvia. Wildfowl. 2019;14:164–77.Charmantier A, Perrins C, McCleery RH, Sheldon BC. Quantitative genetics of age at reproduction in wild swans: Support for antagonistic pleiotropy models of senescence. Proc Natl Acad Sci USA. 2006;103:6587–92.Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Hill SC, Hansen R, Watson S, Coward V, Russell C, Cooper J, et al. Comparative micro-epidemiology of pathogenic avian influenza virus outbreaks in a wild bird population. Philos Trans R Soc B Biol Sci. 2019;374:20180259.Cotten M, Oude Munnink B, Canuti M, Deijs M, Watson SJ, Kellam P, et al. Full genome virus detection in fecal samples using sensitive nucleic acid preparation, deep sequencing, and a novel iterative sequence classification algorithm. PLoS ONE. 2014;9:e93269.Article 
PubMed 
PubMed Central 

Google Scholar 
Boom R, Sol CJA, Salimans MMM, Janses CL, Wertheim Van Dillen PME, Van Der Noordaa J. Rapid and simple method for purification of nucleic acids R. J Clin Microbiol. 1990;28:495–503.Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Endoh D, Mizutani T, Kirisawa R, Maki Y, Saito H, Kon Y, et al. Species-independent detection of RNA virus by representational difference analysis using non-ribosomal hexanucleotides for reverse transcription. Nucleic Acids Res. 2005;33:1–11.Article 

Google Scholar 
Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMB. 2011;17:10–12.
Google Scholar 
Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 2008;18:821–9.Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2014;12:59–60.Article 
PubMed 

Google Scholar 
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–10.Article 
CAS 
PubMed 

Google Scholar 
Langmead B Aligning short sequencing reads with Bowtie. Curr Protoc Bioinforma. 2010; Chapter 11: Unit 11.7.Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinforma Oxf Engl. 2012;28:1647–9.Article 

Google Scholar 
Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30:3059–66.Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol Biol Evol. 2013;30:772–80.Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–7.Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Muhire BM, Varsani A, Martin DP SDT: A virus classification tool based on pairwise sequence alignment and identity calculation. PLoS ONE. 2014;9:e108277.Darriba D, Taboada GL, Doallo R, Posada D. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinforma Oxf Engl. 2011;27:1164–5.Article 
CAS 

Google Scholar 
Stamatakis A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–3.Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Kapoor A, Simmonds P, Lipkin WI, Zaidi S, Delwart E. Use of nucleotide composition analysis to infer hosts for three novel picorna-like viruses. J Virol. 2010;84:10322–8.Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Wood DE, Salzberg SL Kraken: Ultrafast metagenomic sequence classification using exact alignments. Genome Biol. 2014;15:R46.Lu J, Breitwieser FP, Thielen P, Salzberg SL. Bracken: estimating species abundance in metagenomics data. PeerJ Comput Sci. 2017;3:e104.Article 

Google Scholar 
Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, et al. Ribosomal Database Project: Data and tools for high throughput rRNA analysis. Nucleic Acids Res. 2014;42:633–42.Article 

Google Scholar 
R Core Team. R: A Language and Environment for Statistical Computing. 2019. R Foundation for Statistical Computing, Vienna, Austria.RStudio Team. RStudio: Integrated Development for R. 2015. Boston, MA, USA.Dixon P. VEGAN, a package of R functions for community ecology. J Veg Sci. 2003;14:927–30.Article 

Google Scholar 
Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 2001;26:32–46.
Google Scholar 
Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol. 1995;57:289–300.
Google Scholar 
Benjamini Y, Yekutieli D. The control of the false discovery rate in multiple testing under dependency. Ann Stat. 2001;29:1165–88.Article 

Google Scholar 
Oakley BB, Lillehoj HS, Kogut MH, Kim WK, Maurer JJ, Pedroso A, et al. The chicken gastrointestinal microbiome. FEMS Microbiol Lett. 2014;360:100–12.Article 
CAS 
PubMed 

Google Scholar 
Waite DW, Taylor MW. Characterizing the avian gut microbiota: Membership, driving influences, and potential function. Front Microbiol. 2014;5:1–12.Article 

Google Scholar 
Waite DW, Taylor MW. Exploring the avian gut microbiota: Current trends and future directions. Front Microbiol. 2015;6:1–12.Article 

Google Scholar 
Zell R, Delwart E, Gorbalenya AE, Hovi T, King AMQ, Knowles NJ, et al. ICTV virus taxonomy profile: Picornaviridae. J Gen Virol. 2017;98:2421–2.Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Cotmore SF, Agbandje-McKenna M, Canuti M, Chiorini JA, Eis-Hubinger AM, Hughes J, et al. ICTV virus taxonomy profile: Parvoviridae. J Gen Virol. 2019;100:367–8.Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Bosch A, Guix S, Krishna N, Méndez E, Monroe SS, Pantin-Jackwood M, et al. Astroviridae. In: King A, Adams M, Carstens E, Lefkowitz E (eds). Virus taxonomy. Classification and nomenclature of viruses: ninth report of the International Committee on the Taxonomy of Viruses. 2011. Elsevier, London, pp 953-9.Risely A. Applying the core microbiome to understand host–microbe systems. J Anim Ecol. 2020;89:1549–58.Article 
PubMed 

Google Scholar 
Piepenbring AK, Enderlein D, Herzog S, Kaleta EF, Heffels-Redmann U, Ressmeyer S, et al. Pathogenesis of avian bornavirus in experimentally infected Cockatiels. Emerg Infect Dis. 2012;18:234–41.Article 
PubMed 
PubMed Central 

Google Scholar 
Anzil AP, Blinzinger K, Mayr A. Persistent Borna virus infection in adult hamsters. Arch Für Gesamt Virusforsch. 1973;40:52–57.Article 
CAS 

Google Scholar 
Heffels-Redmann U, Enderlein D, Herzog S, Piepenbring A, Bürkle M, Neumann D, et al. Follow-Up Investigations on Different Courses of Natural Avian Bornavirus Infections in Psittacines. Avian Dis. 2012;56:153–9.Article 
PubMed 

Google Scholar 
Rubbenstroth D, Brosinski K, Rinder M, Olbert M, Kaspers B, Korbel R, et al. No contact transmission of avian bornavirus in experimentally infected cockatiels (Nymphicus hollandicus) and domestic canaries (Serinus canaria forma domestica). Vet Microbiol. 2014;172:146–56.Article 
PubMed 

Google Scholar 
Olsen I The Family Fusobacteriaceae. In: Rosenberg E, Delong EF, Lory S, Stackebrandt E, Thompson F (eds). The Prokaryotes: Firmicutes and Tenericutes, 4th ed. 2014. pp 109-32.Imhoff JF The Family Chlorobiaceae. In: Rosenberg E, Delong EF, Lory S, Stackebrandt E, Thompson F (eds). The Prokaryotes: Other Major Lineages of Bacteria and The Archaea, 4th ed. 2014. pp 501-14.Cho JC The Family Lentisphaeraceae. In: Rosenberg E, Delong EF, Lory S, Stackebrandt E, Thompson F (eds). The Prokaryotes: Other Major Lineages of Bacteria and The Archaea, 4th ed. 2014. pp 705-10.Karami A, Sarshar M, Ranjbar R, Zanjani RS The Phylum Spirochaetaceae. In: Rosenberg E, Delong EF, Lory S, Stackebrandt E, Thompson F (eds). The Prokaryotes: Other Major Lineages of Bacteria and The Archaea, 4th ed. 2014. pp 915-29.McBride MJ The Family Flavobacteriaceae. In: Rosenberg E, Delong EF, Lory S, Stackebrandt E, Thompson F (eds). The Prokaryotes: Other Major Lineages of Bacteria and The Archaea, 4th ed. 2014. pp 643-76.Van Dijk JGB, Hoye BJ, Verhagen JH, Nolet BA, Fouchier RAM, Klaassen M. Juveniles and migrants as drivers for seasonal epizootics of avian influenza virus. J Anim Ecol. 2014;83:266–75.Article 
PubMed 

Google Scholar 
Chevalier V, Marsot M, Molia S, Rasamoelina H, Rakotondravao R, Pedrono M, et al. Serological evidence of West Nile and Usutu viruses circulation in domestic and wild birds in wetlands of Mali and Madagascar in 2008. Int J Environ Res Public Health. 2020;17:1998.Guy, JS Turkey Viral Hepatitis. Diseases of Poultry, 12th Edition. 2008. Wiley Blackwell, pp 426-30.Davies ZG, Fuller RA, Dallimer M, Loram A, Gaston KJ. Household factors influencing participation in bird feeding activity: a national scale analysis. PLOS ONE. 2012;7:e39692.Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Shutt JD, Trivedi UH, Nicholls JA. Faecal metabarcoding reveals pervasive long-distance impacts of garden bird feeding. Proc R Soc B Biol Sci. 2021;288:20210480.Article 

Google Scholar 
Minich JJ, Sanders JG, Amir A, Humphrey G, Gilbert JA, Knight R. Quantifying and understanding well-to-well contamination in microbiome research. mSystems. 2019;4:e00186–19.Article 
PubMed 
PubMed Central 

Google Scholar  More

Surface energy fluxes and componentsIn our study, we focused on the circumpolar land north of 60° latitude, and specifically on the extent of the circumpolar Arctic vegetation map (CAVM20, Supplementary Fig. 1–3). We obtained half-hourly and hourly in situ observations of energy fluxes and meteorological variables from the monitoring networks FLUXNET28 (fluxnet.org; FLUXNET2015 dataset), AmeriFlux29 (ameriflux.lbl.gov), AON31,32 (aon.iab.uaf.edu), ICOS (icos-cp.eu), GEM35,36 (g-e-m.dk), GC-Net33,34 (cires1.colorado.edu/steffen/gcnet) and PROMICE30; (promice.dk; Supplementary Table 3). We did not include observations from the Baseline Surface Radiation Network (BSRN; bsrn.awi.de) and Global Energy Balance Archive (GEBA; geba.ethz.ch) because they typically lack information on non-radiative energy fluxes. Finally, we did not include observations from the European Flux Database Cluster (EFDC, europe-fluxdata.eu) because these data are largely located outside the domain of the CAVM20.We aggregated surface energy fluxes and components (Supplementary Table 1) to daily resolution as follows: (i) we extracted only directly measured data and excluded gap-filled data by filtering according to quality information; (ii) we performed a basic outlier filtering (excluding shortwave and longwave radiation flux values >1400 Wm−2 and in case of incoming/outgoing radiation More

Battaglini, L., Bovolenta, S., Gusmeroli, F., Salvador, S. & Sturaro, E. Environmental sustainability of alpine livestock farms. Ital. J. Anim. Sci. 13, 3155 (2014).
Google Scholar 
Lavorel, S. et al. Historical trajectories in land use pattern and grassland ecosystem services in two European alpine landscapes. Reg. Environ. Change 17, 2251–2264 (2017).PubMed Central 

Google Scholar 
Pan, Y., Wu, J. & Xu, Z. Analysis of the tradeoffs between provisioning and regulating services from the perspective of varied share of net primary production in an alpine grassland ecosystem. Ecol. Complex. 17, 79–86 (2014).
Google Scholar 
Rossi, M. et al. A comparison of the signal from diverse optical sensors for monitoring alpine grassland dynamics. Remote Sens. 11, 296 (2019).ADS 

Google Scholar 
Körner, C. Plant ecology at high elevations. In Alpine Plant Life: Functional Plant Ecology of High Mountain Ecosystems (ed. Körner, C.) 1–7 (Springer, 2003). https://doi.org/10.1007/978-3-642-18970-8_1.Jonas, T., Rixen, C., Sturm, M. & Stoeckli, V. How alpine plant growth is linked to snow cover and climate variability. J. Geophys. Res. Biogeosci. 113 (2008).Körner, C. Impact of atmospheric changes on high mountain vegetation. In Mountain Environments in Changing Climates 155–166 (Routledge, 1994).Choler, P. Growth response of temperate mountain grasslands to inter-annual variations in snow cover duration. Biogeosciences 12, 3885–3897 (2015).ADS 

Google Scholar 
Schirmer, M., Wirz, V., Clifton, A. & Lehning, M. Persistence in intra-annual snow depth distribution: 1. Measurements and topographic control. Water Resour. Res. 47, 09516 (2011).ADS 

Google Scholar 
Revuelto, J., Jonas, T. & López-Moreno, J.-I. Backward snow depth reconstruction at high spatial resolution based on time-lapse photography. Hydrol. Process. 30, 2976–2990 (2016).ADS 

Google Scholar 
López-Moreno, J. I. et al. Small scale spatial variability of snow density and depth over complex alpine terrain: Implications for estimating snow water equivalent. Adv. Water Resour. 55, 40–52 (2013).ADS 

Google Scholar 
Clark, M. P. et al. Representing spatial variability of snow water equivalent in hydrologic and land-surface models: A review. Water Resour. Res. 47, (2011).Wayand, N. E., Hamlet, A. F., Hughes, M., Feld, S. I. & Lundquist, J. D. Intercomparison of meteorological forcing data from empirical and mesoscale model sources in the north fork american river basin in northern sierra Nevada, California. J. Hydrometeorol. 14, 677–699 (2013).ADS 

Google Scholar 
Revuelto, J., López-Moreno, J. I., Azorin-Molina, C. & Vicente-Serrano, S. M. Topographic control of snowpack distribution in a small catchment in the central Spanish Pyrenees: Intra- and inter-annual persistence. Cryosphere 8, 1989–2006 (2014).ADS 

Google Scholar 
Winkler, D. E., Butz, R. J., Germino, M. J., Reinhardt, K. & Kueppers, L. M. Snowmelt timing regulates community composition, phenology, and physiological performance of alpine plants. Front. Plant Sci. (2018).Scherrer, D. & Körner, C. Topographically controlled thermal-habitat differentiation buffers alpine plant diversity against climate warming. J. Biogeogr. 38, 406–416 (2011).
Google Scholar 
Billings, W. D. Arctic and alpine vegetations: Similarities, differences, and susceptibility to disturbance. Bioscience 23, 697–704 (1973).
Google Scholar 
Hua, X., Ohlemüller, R. & Sirguey, P. Differential effects of topography on the timing of the growing season in mountainous grassland ecosystems. Environ. Adv. 8, 100234 (2022).
Google Scholar 
Xie, J. et al. Land surface phenology and greenness in Alpine grasslands driven by seasonal snow and meteorological factors. Sci. Total Environ. 725, 138380 (2020).ADS 
CAS 

Google Scholar 
Carlson, B. Z., Choler, P., Renaud, J., Dedieu, J.-P. & Thuiller, W. Modelling snow cover duration improves predictions of functional and taxonomic diversity for alpine plant communities. Ann. Bot. 116, 1023–1034 (2015).PubMed Central 

Google Scholar 
Beniston, M. et al. The European mountain cryosphere: A review of its current state, trends, and future challenges. Cryosphere 12, 759–794 (2018).ADS 

Google Scholar 
Stöckli, R. & Vidale, P. L. European plant phenology and climate as seen in a 20-year AVHRR land-surface parameter dataset. Int. J. Remote Sens. 25, 3303–3330 (2004).
Google Scholar 
Steinbauer, M. J. et al. Accelerated increase in plant species richness on mountain summits is linked to warming. Nature 556, 231–234 (2018).ADS 
CAS 

Google Scholar 
Fazeli Farsani, I., Farzaneh, M. R., Besalatpour, A. A., Salehi, M. H. & Faramarzi, M. Assessment of the impact of climate change on spatiotemporal variability of blue and green water resources under CMIP3 and CMIP5 models in a highly mountainous watershed. Theor. Appl. Climatol. 136, 169–184 (2019).ADS 

Google Scholar 
Kharin, V. V., Zwiers, F. W., Zhang, X. & Wehner, M. Changes in temperature and precipitation extremes in the CMIP5 ensemble. Clim. Change 119, 345–357 (2013).ADS 

Google Scholar 
Engler, R. et al. 21st century climate change threatens mountain flora unequally across Europe. Glob. Change Biol. 17, 2330–2341 (2011).ADS 

Google Scholar 
Qiao, D. & Wang, N. Relationship between winter snow cover dynamics, climate and spring grassland vegetation phenology in Inner Mongolia, China. ISPRS Int. J. Geo-Inf. 8, 42 (2019).
Google Scholar 
Zong, S. et al. Upward range shift of a dominant alpine shrub related to 50 years of snow cover change. Remote Sens. Environ. 268, 112773 (2022).ADS 

Google Scholar 
Ernakovich, J. G. et al. Predicted responses of arctic and alpine ecosystems to altered seasonality under climate change. Glob. Change Biol. 20, 3256–3269 (2014).ADS 

Google Scholar 
Zheng, J., Jia, G. & Xu, X. Earlier snowmelt predominates advanced spring vegetation greenup in Alaska. Agric. For. Meteorol. 315, 108828 (2022).ADS 

Google Scholar 
Dedieu, J.-P. et al. On the importance of high-resolution time series of optical imagery for quantifying the effects of snow cover duration on alpine plant habitat. Remote Sens. 8, 481 (2016).ADS 

Google Scholar 
Virtanen, T. & Ek, M. The fragmented nature of tundra landscape. Int. J. Appl. Earth Obs. Geoinf. 27, 4–12 (2014).ADS 

Google Scholar 
Fontana, F., Rixen, C., Jonas, T., Aberegg, G. & Wunderle, S. Alpine grassland phenology as seen in AVHRR, VEGETATION, and MODIS NDVI time series—A comparison with in situ measurements. Sensors 8, 2833–2853 (2008).ADS 
PubMed Central 

Google Scholar 
Carlson, B. Z. et al. Observed long-term greening of alpine vegetation—A case study in the French Alps. Environ. Res. Lett. 12, 114006 (2017).ADS 

Google Scholar 
Tomaszewska, M. A., Nguyen, L. H. & Henebry, G. M. Land surface phenology in the highland pastures of montane Central Asia: Interactions with snow cover seasonality and terrain characteristics. Remote Sens. Environ. 240, 111675 (2020).ADS 

Google Scholar 
Rumpf, S. B. et al. From white to green: Snow cover loss and increased vegetation productivity in the European Alps. Science 376, 1119–1122 (2022).ADS 
CAS 

Google Scholar 
Myneni, R. B. & Williams, D. L. On the relationship between FAPAR and NDVI. Remote Sens. Environ. 49, 200–211 (1994).ADS 

Google Scholar 
Pettorelli, N. et al. Using the satellite-derived NDVI to assess ecological responses to environmental change. Trends Ecol. Evol. 20, 503–510 (2005).
Google Scholar 
Asam, S. et al. Relationship between spatiotemporal variations of climate, snow cover and plant phenology over the alps—An earth observation-based analysis. Remote Sens. 10, 1757 (2018).ADS 

Google Scholar 
Rossini, M. et al. Remote sensing-based estimation of gross primary production in a subalpine grassland. Biogeosciences 9, 2565–2584 (2012).ADS 

Google Scholar 
Dozier, J. Spectral signature of alpine snow cover from the landsat thematic mapper. Remote Sens. Environ. 28, 9–22 (1989).ADS 

Google Scholar 
Hall, D. K. & Riggs, G. A. Accuracy assessment of the MODIS snow products. Hydrol. Process. 21, 1534–1547 (2007).ADS 

Google Scholar 
Julitta, T. et al. Using digital camera images to analyse snowmelt and phenology of a subalpine grassland. Agric. For. Meteorol. 198–199, 116–125 (2014).ADS 

Google Scholar 
Francon, L. et al. Assessing the effects of earlier snow melt-out on alpine shrub growth: The sooner the better?. Ecol. Ind. 115, 106455 (2020).
Google Scholar 
Assmann, J. J., Myers-Smith, I. H., Kerby, J. T., Cunliffe, A. M. & Daskalova, G. N. Drone data reveal heterogeneity in tundra greenness and phenology not captured by satellites. Environ. Res. Lett. 15, 125002 (2020).ADS 
CAS 

Google Scholar 
Revuelto, J. et al. Meteorological and snow distribution data in the Izas Experimental Catchment (Spanish Pyrenees) from 2011 to 2017. Earth Syst. Sci. Data 9, 993–1005 (2017).ADS 

Google Scholar 
Nadal Romero, E. et al. Sediment balance in four small catechumen’s with different land cover in the Central Pyrenes (Spain). (2009).Gartzia, M., Alados, C. L. & Pérez-Cabello, F. Assessment of the effects of biophysical and anthropogenic factors on woody plant encroachment in dense and sparse mountain grasslands based on remote sensing data. Progr. Phys. Geogr. Earth Environ. 38, 201–217 (2014).
Google Scholar 
Fillat, F., González, R. G., García, D. G., Gómez, D. & Reiné, R. Pastos del Pirineo. (Editorial CSIC-CSIC Press, 2008).Gómez-García, D., Ferrández, J. V., Tejero, P. & Font, X. Spatial distribution and environmental analysis of the alpine flora in the Pyrenees. Pirineos 172, e027–e027 (2017).
Google Scholar 
Gascoin, S. et al. A snow cover climatology for the Pyrenees from MODIS snow products. Hydrol. Earth Syst. Sci. 19, 2337–2351 (2015).ADS 

Google Scholar 
López-Moreno, J. I. et al. Different sensitivities of snowpacks to warming in Mediterranean climate mountain areas. Environ. Res. Lett. 12, 074006 (2017).ADS 

Google Scholar 
Cernusca, A. Standörtliche Variabilität in Mikroklima und Energiehaushalt Alpiner Zwergstrauchbestände. In Verhandlungen der Gesellschaft für Ökologie Wien 1975: 5. Jahresversammlung vom 22. bis 24. September 1975 in Wien (ed. Müller, P.) 9–21 (Springer Netherlands, 1976). https://doi.org/10.1007/978-94-015-7168-5_2.Cernusca, A. & Seeber, M. C. Canopy structure, microclimate and the energy budget in different alpine plant communities. In Symposium—British Ecological Society (1981).Kudo, G., Nordenhäll, U. & Molau, U. Effects of snowmelt timing on leaf traits, leaf production, and shoot growth of alpine plants: Comparisons along a snowmelt gradient in northern Sweden. Écoscience 6, 439–450 (1999).
Google Scholar 
Baptist, F. & Choler, P. A simulation of the importance of length of growing season and canopy functional properties on the seasonal gross primary production of temperate alpine meadows. Ann. Bot. 101, 549–559 (2008).PubMed Central 

Google Scholar 
Baptist, F., Flahaut, C., Streb, P. & Choler, P. No increase in alpine snowbed productivity in response to experimental lengthening of the growing season. Plant Biol. 12, 755–764 (2010).CAS 

Google Scholar 
Wipf, S., Rixen, C. & Mulder, C. P. H. Advanced snowmelt causes shift towards positive neighbour interactions in a subarctic tundra community. Glob. Change Biol. 12, 1496–1506 (2006).ADS 

Google Scholar 
Sierra-Almeida, A. & Cavieres, L. A. Summer freezing resistance decreased in high-elevation plants exposed to experimental warming in the central Chilean Andes. Oecologia 163, 267–276 (2010).ADS 

Google Scholar 
Camarero, J. J., Gutiérrez, E. & Fortin, M.-J. Spatial pattern of subalpine forest-alpine grassland ecotones in the Spanish Central Pyrenees. For. Ecol. Manag. 134, 1–16 (2000).
Google Scholar 
Dadic, R., Mott, R., Lehning, M. & Burlando, P. Parameterization for wind-induced preferential deposition of snow. Hydrol. Process. 24, 1994–2006 (2010).
Google Scholar 
Vionnet, V. et al. Simulation of wind-induced snow transport and sublimation in alpine terrain using a fully coupled snowpack/atmosphere model. Cryosphere 8, 395–415 (2014).ADS 

Google Scholar 
Burns, S. F., Tonkin, P. J. & Thorn, C. E. Soil-geomorphic models and the spatial distribution and development of alpine soils. In Space and Time in Geomorphology: Binghamton Geomorphology Symposium, vol. 12 (2020).Lana-Renault, N. et al. Comparative analysis of the response of various land covers to an exceptional rainfall event in the central Spanish Pyrenees, October 2012. Earth Surf. Proc. Land. 39, 581–592 (2014).ADS 

Google Scholar 
Freppaz, M., Williams, B. L., Edwards, A. C., Scalenghe, R. & Zanini, E. Simulating soil freeze/thaw cycles typical of winter alpine conditions: Implications for N and P availability. Appl. Soil. Ecol. 35, 247–255 (2007).
Google Scholar 
López-Moreno, J. I. et al. Long-term trends (1958–2017) in snow cover duration and depth in the Pyrenees. Int. J. Climatol. 40, 6122–6136 (2020).
Google Scholar 
López-Moreno, J. I., Vicente-Serrano, S. M. & Lanjeri, S. Mapping snowpack distribution over large areas using GIS and interpolation techniques. Clim. Res. 33, 257–270 (2007).
Google Scholar 
Revuelto, J., López-Moreno, J. I. & Alonso-González, E. Light and shadow in mapping alpine snowpack with unmanned aerial vehicles in the absence of ground control points. Water Resour. Res. 57, e2020WR028980 (2021).ADS 

Google Scholar 
Eberhard, L. A. et al. Intercomparison of photogrammetric platforms for spatially continuous snow depth mapping. Cryosphere 15, 69–94 (2021).ADS 

Google Scholar 
Harder, P., Schirmer, M., Pomeroy, J. & Helgason, W. Accuracy of snow depth estimation in mountain and prairie environments by an unmanned aerial vehicle. Cryosphere 10, 2559–2571 (2016).ADS 

Google Scholar 
Stanton, M. L., Rejmánek, M. & Galen, C. Changes in vegetation and soil fertility along a predictable snowmelt gradient in the mosquito range, Colorado, USA. Arct. Alp. Res. 26, 364–374 (1994).
Google Scholar 
Winkler, D. E., Chapin, K. J. & Kueppers, L. M. Soil moisture mediates alpine life form and community productivity responses to warming. Ecology 97, 1553–1563 (2016).
Google Scholar 
Litaor, M. I., Williams, M. & Seastedt, T. R. Topographic controls on snow distribution, soil moisture, and species diversity of herbaceous alpine vegetation, Niwot Ridge, Colorado. J. Geophys. Res. Biogeosci. 113, (2008).Keller, F., Kienast, F. & Beniston, M. Evidence of response of vegetation to environmental change on high-elevation sites in the Swiss Alps. Reg. Environ. Change 1, 70–77 (2000).
Google Scholar 
Running, S. W. Estimating terrestrial primary productivity by combining remote sensing and ecosystem simulation. In Remote Sensing of Biosphere Functioning (eds. Hobbs, R. J. & Mooney, H. A.) 65–86 (Springer, 1990). https://doi.org/10.1007/978-1-4612-3302-2_4.Myneni, R. B., Hall, F. G., Sellers, P. J. & Marshak, A. L. The interpretation of spectral vegetation indexes. IEEE Trans. Geosci. Remote Sens. 33, 481–486 (1995).ADS 

Google Scholar 
Huang, S., Tang, L., Hupy, J. P., Wang, Y. & Shao, G. A commentary review on the use of normalized difference vegetation index (NDVI) in the era of popular remote sensing. J. For. Res. 32, 1–6 (2021).
Google Scholar 
Floyd, D. A. & Anderson, J. E. A comparison of three methods for estimating plant cover. J. Ecol. 75, 221–228 (1987).
Google Scholar 
Peet, R. K. The measurement of species diversity. Annu. Rev. Ecol. Syst. 5, 285–307 (1974).
Google Scholar 
Mouillot, D. & Leprêtre, A. A comparison of species diversity estimators. Res. Popul. Ecol. 41, 203–215 (1999).
Google Scholar  More

Allsop, K. A. & Miller, J. B. Honey revisited: A reappraisal of honey in pre-industrial diets. Br. J. Nutr. 75, 513–520 (1996).Article 
CAS 
PubMed 

Google Scholar 
Dams, M. & Dams, L. Spanish rock art depicting honey gathering during the Mesolithic. Nature 268, 228–230 (1977).Article 
ADS 

Google Scholar 
Bradbear, N. Bees and their role in forest livelihoods: A guide to the services provided by bees and the sustainable harvesting, processing and marketing of their products. Non-Wood Forests Products Series, Vol. 19 (FAO, Rome, 2009).
Google Scholar 
Crane, E. The World History of Beekeeping and Honey Hunting (Routledge, 1999).Book 

Google Scholar 
Kritsky, G. Beekeeping from Antiquity through the middle ages. Annu. Rev. Entomol. 62, 249–264 (2017).Article 
CAS 
PubMed 

Google Scholar 
Grüter, C. Stingless Bees: Their Behaviour, Ecology and Evolution (Springer International Publishing, 2020).Book 

Google Scholar 
Weaver, N. & Weaver, E. C. Beekeeping with the stingless bee Melipona beecheii, by the Yucatecan Maya. Bee World 62, 7–19 (1981).Article 

Google Scholar 
Quezada-Euán, J. J. G. Stingless Bees of Mexico: The Biology, Management and Conservation of an Ancient Heritage (Springer, 2018).Book 

Google Scholar 
Medellín Morales, S. Meliponicultura Maya: Perspectivas para su sostenibilidad. Reporte de sostenibilidad Maya no. 2; 67 pp. (1991).González-Acereto, J. A. La meliponicultura yucateca en crisis: Una actividad indígena a punto de desaparecer, 1er Seminario Nacional sobre Abejas sin Aguijón. Boca Río Ver México 9–12 (1999).Russell, P. The History of Mexico: From Pre-conquest to Present (Routledge, 2010).
Google Scholar 
Quezada-Euan, J. J., May-Itzá, W. & González-Acereto, J. Meliponiculture in Mexico: Problems and perspective for development. Bee World 82, 160–167 (2001).Article 

Google Scholar 
Freitas, B. M. et al. Diversity, threats and conservation of native bees in the Neotropics. Apidologie 40, 332–346 (2009).Article 

Google Scholar 
Toledo-Hernández, E. et al. The stingless bees (Hymenoptera: Apidae: Meliponini): A review of the current threats to their survival. Apidologie 53, 8 (2022).Article 

Google Scholar 
Guzman-Novoa, E. et al. The process and outcome of the Africanization of honey bees in Mexico: Lessons and future directions. Front. Ecol. Evol. 8, 404 (2020).Article 

Google Scholar 
Fletcher, M. et al. Stingless bee honey, a novel source of trehalulose: A biologically active disaccharide with health benefits. Sci. Rep. 10, 12128 (2020).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Rao, P. V., Krishnan, K. T., Salleh, N. & Gan, S. H. Biological and therapeutic effects of honey produced by honey bees and stingless bees: A comparative review. Rev. Bras. Farmacogn. 26, 657–664 (2016).Article 
CAS 

Google Scholar 
Rattanawannee, A. & Duangphakdee, O. Southeast Asian meliponiculture for sustainable livelihood. In Modern Beekeeping – Bases for Sustainable Production (ed. Ranz, R. E. R.) (IntechOpen, 2019).
Google Scholar 
Heard, T. The role of stingless bees in crop pollination. Annu. Rev. Entomol. 44, 183–206 (1999).Article 
CAS 
PubMed 

Google Scholar 
Slaa, E. J., Chaves, L. A. S., Malagodi-Braga, K. S. & Hofstede, F. E. Stingless bees in applied pollination: Practice and perspectives. Apidologie 37, 293–315 (2006).Article 

Google Scholar 
Kendall, L. K., Stavert, J. R., Gagic, V., Hall, M. & Rader, R. Initial floral visitor identity and foraging time strongly influence blueberry reproductive success. Basic Appl. Ecol. https://doi.org/10.1016/j.baae.2022.02.009 (2022).Article 

Google Scholar 
Kiatoko, N. et al. Effective pollination of greenhouse Galia musk melon (Cucumis melo L. var. reticulatus ser.) by afrotropical stingless bee species. J. Apic. Res. https://doi.org/10.1080/00218839.2021.2021641 (2022).Article 

Google Scholar 
Nkoba, K. et al. African endemic stingless bees as an efficient alternative pollinator to honey bees in greenhouse cucumber (Cucumis sativus L.). J. Apic. Res. https://doi.org/10.1080/00218839.2021.2013421 (2022).Article 

Google Scholar 
FAO, A. Good beekeeping practices for sustainable apiculture. (FAO, IZSLT, Apimondia and CAAS, 2020). doi:https://doi.org/10.4060/cb5353en.Patel, V., Pauli, N., Biggs, E., Barbour, L. & Boruff, B. Why bees are critical for achieving sustainable development. Ambio 50, 49–59 (2021).Article 
PubMed 

Google Scholar 
Fuller, D. Q. et al. Convergent evolution and parallelism in plant domestication revealed by an expanding archaeological record. Proc. Natl. Acad. Sci. 111, 6147–6152 (2014).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Purugganan, M. D. An evolutionary genomic tale of two rice species. Nat. Genet. 46, 931–932 (2014).Article 
CAS 
PubMed 

Google Scholar 
Kleisner, K. & Stella, M. Monsters we met, monsters we made: On the parallel emergence of phenotypic similarity under domestication. Σημειωτκή – Sign Syst. Stud. 37, 454–476 (2009).Article 

Google Scholar 
Wilkins, A. S., Wrangham, R. W. & Fitch, W. T. The, “Domestication Syndrome” in mammals: A unified explanation based on neural crest cell behavior and genetics. Genetics 197, 795–808 (2014).Article 
PubMed 
PubMed Central 

Google Scholar 
Lecocq, T. Insects: The disregarded domestication histories. In Animal Domestication (ed. Teletchea, F.) (IntechOpen, 2018).
Google Scholar 
Pollan, M. The botany of desire: A plant’s-eye view of the world. Econ. Bot. 57(1), 146–147 (2002).
Google Scholar 
Chuttong, B., Chanbang, Y., Sringarm, K. & Burgett, M. Physicochemical profiles of stingless bee (Apidae: Meliponini) honey from South East Asia (Thailand). Food Chem. 192, 149–155 (2016).Article 
CAS 
PubMed 

Google Scholar 
Spivak, M. & Danka, R. G. Perspectives on hygienic behavior in Apis mellifera and other social insects. Apidologie 52, 1–16 (2021).Article 

Google Scholar 
Breed, M. D., Guzmán-Novoa, E. & Hunt, G. J. 3. Defensive behavior of honey bees: Organization, genetics, and comparisons with other bees. Annu. Rev. Entomol. 49, 271–298 (2004).Article 
CAS 
PubMed 

Google Scholar 
Hunt, G. J. et al. Behavioral genomics of honeybee foraging and nest defense. Naturwissenschaften 94, 247–267 (2007).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Faegri, K. & van der Pijl,. Principles of Pollination Ecology (Pergamon Press, 1979).
Google Scholar 
Nicolson, S. W. & Thornburg, R. W. Nectar chemistry. In Nectaries and Nectar (eds Nicolson, S. W. et al.) (Springer Netherlands, 2007).Chapter 

Google Scholar 
Abrahamczyk, S. et al. Pollinator adaptation and the evolution of floral nectar sugar composition. J. Evol. Biol. 30, 112–127 (2017).Article 
CAS 
PubMed 

Google Scholar 
Parachnowitsch, A. L., Manson, J. S. & Sletvold, N. Evolutionary ecology of nectar. Ann. Bot. 123, 247–261 (2019).Article 
CAS 
PubMed 

Google Scholar 
Rasmussen, C. & Cameron, S. A. Global stingless bee phylogeny supports ancient divergence, vicariance, and long distance dispersal. Biol. J. Linn. Soc. 99, 206–232 (2010).Article 

Google Scholar 
Bantle, J. P. Dietary fructose and metabolic syndrome and diabetes. J. Nutr. 139, 1263S-1268S (2009).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Erejuwa, O. O., Sulaiman, S. A. & Wahab, M. S. A. fructose might contribute to the hypoglycemic effect of honey. Molecules 17, 1900–1915 (2012).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Kwakman, P. H. S. & Zaat, S. A. J. Antibacterial components of honey. IUBMB Life 64, 48–55 (2012).Article 
CAS 
PubMed 

Google Scholar 
Viuda-Martos, M., Ruiz-Navajas, Y., Fernández-López, J. & Pérez-Álvarez, J. A. Functional properties of honey, propolis, and royal jelly. J. Food Sci. 73, R117–R124 (2008).Article 
CAS 
PubMed 

Google Scholar 
Machado De-Melo, A. A., de Almeida-Muradian, L. B., Sancho, M. T. & Pascual-Maté, A. Composition and properties of Apis mellifera honey: A review. J. Apic. Res. 57, 5–37 (2018).Article 

Google Scholar 
Nordin, A., Sainik, N. Q. A. V., Chowdhury, S. R., Saim, A. B. & Idrus, R. B. H. Physicochemical properties of stingless bee honey from around the globe: A comprehensive review. J. Food Compos. Anal. 73, 91–102 (2018).Article 
CAS 

Google Scholar 
Viteri, R., Zacconi, F., Montenegro, G. & Giordano, A. Bioactive compounds in Apis mellifera monofloral honeys. J. Food Sci. 86, 1552–1582 (2021).Article 
CAS 
PubMed 

Google Scholar 
Bueno, F. G. B. et al. Stingless bee floral visitation in the global tropics and subtropics. BioRxiv. https://doi.org/10.1101/2021.04.26.440550 (2021).Article 
PubMed 
PubMed Central 

Google Scholar 
Rasmussen, C. & Cameron, S. A. A molecular phylogeny of the Old World stingless bees (Hymenoptera: Apidae: Meliponini) and the non-monophyly of the large genus Trigona. Syst. Entomol. 32, 26–39 (2007).Article 

Google Scholar 
Mokaya, H. O., Nkoba, K., Ndunda, R. M. & Vereecken, N. J. Characterization of honeys produced by sympatric species of Afrotropical stingless bees (Hymenoptera, Meliponini). Food Chem. 366, 130597 (2022).Article 
CAS 
PubMed 

Google Scholar 
Souza, E. C. A., Menezes, C. & Flach, A. Stingless bee honey (Hymenoptera, Apidae, Meliponini): A review of quality control, chemical profile, and biological potential. Apidologie 52, 113–132 (2021).Article 

Google Scholar 
Ohmenhaeuser, M., Monakhova, Y. B., Kuballa, T. & Lachenmeier, D. W. Qualitative and quantitative control of honeys using NMR spectroscopy and chemometrics. ISRN Anal. Chem. 2013, 1–9 (2013).Article 

Google Scholar 
Mazzoni, V., Bradesi, P., Tomi, F. & Casanova, J. Direct qualitative and quantitative analysis of carbohydrate mixtures using 13C NMR spectroscopy: Application to honey. Magn. Reson. Chem. 35, S81–S90 (1997).Article 
CAS 

Google Scholar 
Consonni, R. & Cagliani, L. R. Geographical characterization of polyfloral and acacia honeys by nuclear magnetic resonance and chemometrics. J. Agric. Food Chem. 56, 6873–6880 (2008).Article 
CAS 
PubMed 

Google Scholar 
Schievano, E., Peggion, E. & Mammi, S. H1 nuclear magnetic resonance spectra of chloroform extracts of honey for chemometric determination of its botanical origin. J. Agric. Food Chem. 58, 57–65 (2010).Article 
CAS 
PubMed 

Google Scholar 
RStudio Team. RStudio: Integrated Development Environment for R. Rstudio, PBC, Boston, MA. URL http://www.rstudio.com (2020).R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/ (2021).Oksanen J., et al. Vegan: Community ecology package. McGlinn lab URL https://CRAN.R-project.org/package=vegan (2020).Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, New York, 2016).Book 
MATH 

Google Scholar 
Yu, G. Using ggtree to visualize data on tree-like structures. Curr. Protoc. Bioinforma. 69, e96. https://doi.org/10.1002/cpbi.96 (2020).Article 

Google Scholar 
Cáceres, M. D. & Legendre, P. Associations between species and groups of sites: Indices and statistical inference. Ecology 90, 3566–3574 (2009).Article 
PubMed 

Google Scholar  More