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    Global habitat suitability modeling reveals insufficient habitat protection for mangrove crabs

    Valiela, I., Bowen, J. L. & York, J. K. Mangrove Forests: One of the World’s Threatened Major Tropical Environments: At least 35% of the area of mangrove forests has been lost in the past two decades, losses that exceed those for tropical rain forests and coral reefs, two other well-known threatened environments. Bioscience 51, 807–815. https://doi.org/10.1641/0006-3568(2001)051[0807:MFOOTW]2.0.CO;2 (2001).Article 

    Google Scholar 
    Kuenzer, C., Bluemel, A., Gebhardt, S., Quoc, T. V. & Dech, S. Remote sensing of mangrove ecosystems: A review. Remote Sens. 3, 1. https://doi.org/10.3390/rs3050878 (2011).Article 

    Google Scholar 
    Turschwell, M. P. et al. Multi-scale estimation of the effects of pressures and drivers on mangrove forest loss globally. Biol. Cons. 247, 108637. https://doi.org/10.1016/j.biocon.2020.108637 (2020).Article 

    Google Scholar 
    Millennium Ecosystem Assessment. Ecosystems and Human Well-being: Synthesis. (2005).Nagelkerken, I. et al. The habitat function of mangroves for terrestrial and marine fauna: A review. Aquat. Bot. 89, 155–185. https://doi.org/10.1016/j.aquabot.2007.12.007 (2008).Article 

    Google Scholar 
    Hamilton, S. E. & Casey, D. Creation of a high spatio-temporal resolution global database of continuous mangrove forest cover for the 21st century (CGMFC-21). Glob. Ecol. Biogeogr. 25, 729–738. https://doi.org/10.1111/geb.12449 (2016).Article 

    Google Scholar 
    Friess, D. A. et al. The state of the world’s Mangrove forests: Past, present, and future. Annu. Rev. Environ. Resour. 44, 89–115. https://doi.org/10.1146/annurev-environ-101718-033302 (2019).Article 

    Google Scholar 
    Zeng, Y., Friess, D. A., Sarira, T. V., Siman, K. & Koh, L. P. Global potential and limits of mangrove blue carbon for climate change mitigation. Curr. Biol. 31, 1737-1743.e1733. https://doi.org/10.1016/j.cub.2021.01.070 (2021).Article 
    CAS 

    Google Scholar 
    zu Ermgassen, P. S. E. et al. Fishers who rely on mangroves: Modelling and mapping the global intensity of mangrove-associated fisheries. Estuar. Coast. Shelf Sci. 247, 106975. https://doi.org/10.1016/j.ecss.2020.106975 (2020).Article 

    Google Scholar 
    Walters, A. D. et al. Do hotspots fall within protected areas? A geographic approach to planning analysis of regional freshwater biodiversity. Freshw. Biol. 64, 2046–2056. https://doi.org/10.1111/fwb.13394 (2019).Article 

    Google Scholar 
    Blasco, F., Saenger, P. & Janodet, E. Mangroves as indicators of coastal change. CATENA 27, 167–178. https://doi.org/10.1016/0341-8162(96)00013-6 (1996).Article 

    Google Scholar 
    Gilman, E. L., Ellison, J., Duke, N. C. & Field, C. Threats to mangroves from climate change and adaptation options: A review. Aquat. Bot. 89, 237–250. https://doi.org/10.1016/j.aquabot.2007.12.009 (2008).Article 

    Google Scholar 
    Hamilton, S. Assessing the role of commercial aquaculture in displacing mangrove forest. Bull. Mar. Sci. 89, 585–601 (2013).Article 

    Google Scholar 
    Lovelock, C. E. et al. The vulnerability of Indo-Pacific mangrove forests to sea-level rise. Nature 526, 559–563. https://doi.org/10.1038/nature15538 (2015).Article 
    ADS 
    CAS 

    Google Scholar 
    Richards Daniel, R. & Friess Daniel, A. Rates and drivers of mangrove deforestation in Southeast Asia, 2000–2012. Proc. Natl. Acad. Sci. 113, 344–349. https://doi.org/10.1073/pnas.1510272113 (2016).Article 
    ADS 
    CAS 

    Google Scholar 
    Appeltans, W. et al. The magnitude of global marine species diversity. Curr. Biol. 22, 2189–2202. https://doi.org/10.1016/j.cub.2012.09.036 (2012).Article 
    CAS 

    Google Scholar 
    Ward, R. D., Friess, D. A., Day, R. H. & MacKenzie, R. A. Impacts of climate change on mangrove ecosystems: A region by region overview. Ecosyst. Health Sustain. 2, e01211. https://doi.org/10.1002/ehs2.1211 (2016).Article 

    Google Scholar 
    Van der Stocken, T., Vanschoenwinkel, B., Carroll, D., Cavanaugh, K. C. & Koedam, N. Mangrove dispersal disrupted by projected changes in global seawater density. Nat. Clim. Chang. 12, 685–691. https://doi.org/10.1038/s41558-022-01391-9 (2022).Article 
    ADS 

    Google Scholar 
    Alongi, D. M. The impact of climate change on Mangrove forests. Curr. Clim. Change Rep. 1, 30–39. https://doi.org/10.1007/s40641-015-0002-x (2015).Article 

    Google Scholar 
    Giri, C. et al. Status and distribution of mangrove forests of the world using earth observation satellite data. Glob. Ecol. Biogeogr. 20, 154–159. https://doi.org/10.1111/j.1466-8238.2010.00584.x (2011).Article 

    Google Scholar 
    Kristensen, E. Mangrove crabs as ecosystem engineers; with emphasis on sediment processes. J. Sea Res. 59, 30–43. https://doi.org/10.1016/j.seares.2007.05.004 (2008).Article 
    ADS 

    Google Scholar 
    Penha-Lopes, G. et al. Are fiddler crabs potentially useful ecosystem engineers in mangrove wastewater wetlands?. Mar. Pollut. Bull. 58, 1694–1703. https://doi.org/10.1016/j.marpolbul.2009.06.015 (2009).Article 
    CAS 

    Google Scholar 
    Sharifian, S., Kamrani, E. & Saeedi, H. Global biodiversity and biogeography of mangrove crabs: Temperature, the key driver of latitudinal gradients of species richness. J. Therm. Biol 92, 102692. https://doi.org/10.1016/j.jtherbio.2020.102692 (2020).Article 
    CAS 

    Google Scholar 
    Phillips, S. J., Anderson, R. P. & Schapire, R. E. Maximum entropy modeling of species geographic distributions. Ecol. Model. 190, 231–259. https://doi.org/10.1016/j.ecolmodel.2005.03.026 (2006).Article 

    Google Scholar 
    Guisan, A. & Zimmermann, N. E. Predictive habitat distribution models in ecology. Ecol. Model. 135, 147–186. https://doi.org/10.1016/S0304-3800(00)00354-9 (2000).Article 

    Google Scholar 
    Guisan, A. et al. Predicting species distributions for conservation decisions. Ecol. Lett. 16, 1424–1435. https://doi.org/10.1111/ele.12189 (2013).Article 

    Google Scholar 
    Guisan, A., Thuiller, W. & Zimmermann, N. E. Habitat Suitability and Distribution Models: With Applications in R. (Cambridge University Press, 2017).Luan, J., Zhang, C., Xu, B., Xue, Y. & Ren, Y. Modelling the spatial distribution of three Portunidae crabs in Haizhou Bay, China. PLoS ONE 13, e0207457. https://doi.org/10.1371/journal.pone.0207457 (2018).Article 
    CAS 

    Google Scholar 
    Kafash, A. et al. The Gray Toad-headed Agama, Phrynocephalus scutellatus, on the Iranian Plateau: The degree of niche overlap depends on the phylogenetic distance. Zool. Middle East 64, 47–54. https://doi.org/10.1080/09397140.2017.1401309 (2018).Article 

    Google Scholar 
    Yousefi, M., Shabani, A. A. & Azarnivand, H. Reconstructing distribution of the Eastern Rock Nuthatch during the Last Glacial Maximum and Last Interglacial. Avian Biol. Res. 13, 3–9. https://doi.org/10.1177/1758155919874537 (2019).Article 

    Google Scholar 
    De Rock, P. et al. Predicting large-scale habitat suitability for cetaceans off Namibia using MinxEnt. Mar. Ecol. Prog. Ser. 619, 149–167 (2019).Article 
    ADS 

    Google Scholar 
    Saeedi, H., Basher, Z. & Costello, M. J. Modelling present and future global distributions of razor clams (Bivalvia: Solenidae). Helgol. Mar. Res. 70, 23. https://doi.org/10.1186/s10152-016-0477-4 (2016).Article 

    Google Scholar 
    Bosso, L. et al. The rise and fall of an alien: why the successful colonizer Littorina saxatilis failed to invade the Mediterranean Sea. Biol. Invas. 24, 3169–3187. https://doi.org/10.1007/s10530-022-02838-y (2022).Article 

    Google Scholar 
    Moradmand, M. & Yousefi, M. Ecological niche modelling and climate change in two species groups of huntsman spider genus Eusparassus in the Western Palearctic. Sci. Rep. 12, 4138. https://doi.org/10.1038/s41598-022-08145-9 (2022).Article 
    ADS 
    CAS 

    Google Scholar 
    Compton, T. J., Leathwick, J. R. & Inglis, G. J. Thermogeography predicts the potential global range of the invasive European green crab (Carcinus maenas). Divers. Distrib. 16, 243–255. https://doi.org/10.1111/j.1472-4642.2010.00644.x (2010).Article 

    Google Scholar 
    Kafash, A., Ashrafi, S. & Yousefi, M. Modeling habitat suitability of bats to identify high priority areas for field monitoring and conservation. Environ. Sci. Pollut. Res. 29, 25881–25891. https://doi.org/10.1007/s11356-021-17412-7 (2022).Article 

    Google Scholar 
    Leathwick, J. et al. Novel methods for the design and evaluation of marine protected areas in offshore waters. Conserv. Lett. 1, 91–102. https://doi.org/10.1111/j.1755-263X.2008.00012.x (2008).Article 

    Google Scholar 
    Charrua, A. B., Bandeira, S. O., Catarino, S., Cabral, P. & Romeiras, M. M. Assessment of the vulnerability of coastal mangrove ecosystems in Mozambique. Ocean Coast. Manag. 189, 105145. https://doi.org/10.1016/j.ocecoaman.2020.105145 (2020).Article 

    Google Scholar 
    Khajoei Nasab, F., Mehrabian, A. & Mostafavi, H. Mapping the current and future distributions of Onosma species endemic to Iran. J. Arid Land 12, 1031–1045. https://doi.org/10.1007/s40333-020-0080-z (2020).Article 

    Google Scholar 
    Allyn, A. J. et al. Comparing and synthesizing quantitative distribution models and qualitative vulnerability assessments to project marine species distributions under climate change. PLoS ONE 15, e0231595. https://doi.org/10.1371/journal.pone.0231595 (2020).Article 
    CAS 

    Google Scholar 
    Makki, T., Mostafavi, H., Matkan, A. & Aghighi, H. Modelling Climate-Change Impact on the Spatial Distribution of Garra Rufa (Heckel, 1843) (Teleostei: Cyprinidae). Iran. J. Sci. Technol. Trans. A: Sci. 45, 795–804. https://doi.org/10.1007/s40995-021-01088-2 (2021).Article 

    Google Scholar 
    Bolon, I. et al. What is the impact of snakebite envenoming on domestic animals? A nation-wide community-based study in Nepal and Cameroon. Toxicon: X 9–10, 100068. https://doi.org/10.1016/j.toxcx.2021.100068 (2021).Sharma, A., Dubey, V. K., Johnson, J. A., Rawal, Y. K. & Sivakumar, K. Is there always space at the top? Ensemble modeling reveals climate-driven high-altitude squeeze for the vulnerable snow trout Schizothorax richardsonii in Himalaya. Ecol. Ind. 120, 106900. https://doi.org/10.1016/j.ecolind.2020.106900 (2021).Article 

    Google Scholar 
    Yousefi, M., Naderloo, R. & Keikhosravi, A. Freshwater crabs of the Near East: Increased extinction risk from climate change and underrepresented within protected areas. Glob. Ecol. Conserv. 38, e02266. https://doi.org/10.1016/j.gecco.2022.e02266 (2022).Article 

    Google Scholar 
    Sheykhi Ilanloo, S. et al. Applying opportunistic observations to model current and future suitability of the Kopet Dagh Mountains for a Near Threatened avian scavenger. Avian Biol. Res. 14, 18–26. https://doi.org/10.1177/1758155920962750 (2020).Article 

    Google Scholar 
    Naderloo, R. Grapsoid crabs (Decapoda: Brachyura: Thoracotremata) of the Persian Gulf and the Gulf of Oman. Zootaxa 3048(1), 1. https://doi.org/10.11646/zootaxa.3048.1.1 (2011).Article 

    Google Scholar 
    Naderloo, R. Atlas of crabs of the Persian Gulf. (2017).Innocenti, G., Schubart, C. D. & Fratini, S. Description of Metopograpsus cannicci, new species, a pseudocryptic crab species from East Africa and the Western Indian Ocean (Decapoda: Brachyura: Grapsidae). Raffles Bull. Zool. (RBZ) 68, 619–628 (2020).
    Google Scholar 
    Hemmati, M. R., Shojaei, M. G., Taheri Mirghaed, A., Mashhadi Farahani, M. & Weigt, M. Food sources for camptandriid crabs in an arid mangrove ecosystem of the Persian Gulf: a stable isotope approach. Isotop. Environ. Health Stud. 57, 457–469. https://doi.org/10.1080/10256016.2021.1925665 (2021).Article 
    CAS 

    Google Scholar 
    Tittensor, D. P. et al. Global patterns and predictors of marine biodiversity across taxa. Nature 466, 1098–1101. https://doi.org/10.1038/nature09329 (2010).Article 
    ADS 
    CAS 

    Google Scholar 
    Kordas, R. L., Harley, C. D. G. & O’Connor, M. I. Community ecology in a warming world: The influence of temperature on interspecific interactions in marine systems. J. Exp. Mar. Biol. Ecol. 400, 218–226. https://doi.org/10.1016/j.jembe.2011.02.029 (2011).Article 

    Google Scholar 
    Hall, S. & Thatje, S. Temperature-driven biogeography of the deep-sea family Lithodidae (Crustacea: Decapoda: Anomura) in the Southern Ocean. Polar Biol. 34, 363–370. https://doi.org/10.1007/s00300-010-0890-0 (2011).Article 

    Google Scholar 
    Hannah, L. Climate Change Biology. Academic Press (2015).Ali, H. et al. Expanding or shrinking? range shifts in wild ungulates under climate change in Pamir-Karakoram mountains, Pakistan. PLoS ONE 16, e0260031. https://doi.org/10.1371/journal.pone.0260031 (2022).Article 
    CAS 

    Google Scholar 
    Yousefi, M. et al. Climate change is a major problem for biodiversity conservation: A systematic review of recent studies in Iran. Contemp. Probl. Ecol. 12, 394–403. https://doi.org/10.1134/S1995425519040127 (2019).Article 

    Google Scholar 
    Doney, S. C. et al. Climate Change Impacts on Marine Ecosystems. Ann. Rev. Mar. Sci. 4, 11–37. https://doi.org/10.1146/annurev-marine-041911-111611 (2011).Article 

    Google Scholar 
    Worm, B. & Lotze, H. K. in Climate Change (Second Edition) (ed Trevor M. Letcher) 195–212 (Elsevier, 2016).Ramírez, F., Afán, I., Davis, L. S. & Chiaradia, A. Climate impacts on global hot spots of marine biodiversity. Sci. Adv. 3, e1601198. https://doi.org/10.1126/sciadv.1601198 (2017).Article 
    ADS 

    Google Scholar 
    Worm, B. et al. Impacts of Biodiversity Loss on Ocean Ecosystem Services. Science 314, 787–790. https://doi.org/10.1126/science.1132294 (2006).Article 
    ADS 
    CAS 

    Google Scholar 
    Lester, S. E. et al. Biological effects within no-take marine reserves: a global synthesis. Mar. Ecol. Prog. Ser. 384, 33–46 (2009).Article 
    ADS 

    Google Scholar 
    Daru, B. H. & le Roux, P. C. Marine protected areas are insufficient to conserve global marine plant diversity. Glob. Ecol. Biogeogr. 25, 324–334. https://doi.org/10.1111/geb.12412 (2016).Article 

    Google Scholar 
    Sala, E. et al. Protecting the global ocean for biodiversity, food and climate. Nature https://doi.org/10.1038/s41586-021-03371-z (2021).Article 

    Google Scholar 
    Embling, C. B. et al. Using habitat models to identify suitable sites for marine protected areas for harbour porpoises (Phocoena phocoena). Biol. Cons. 143, 267–279. https://doi.org/10.1016/j.biocon.2009.09.005 (2010).Article 

    Google Scholar 
    Magris, R. A. & Déstro, G. F. G. Predictive modeling of suitable habitats for threatened marine invertebrates and implications for conservation assessment in Brazil. Braz. J. Oceanogr. 58, 57–68 (2010).Article 

    Google Scholar 
    Welch, H., Pressey, R. L. & Reside, A. E. Using temporally explicit habitat suitability models to assess threats to mobile species and evaluate the effectiveness of marine protected areas. J. Nat. Conserv. 41, 106–115. https://doi.org/10.1016/j.jnc.2017.12.003 (2018).Article 

    Google Scholar 
    Rhoden, C. M., Peterman, W. E. & Taylor, C. A. Maxent-directed field surveys identify new populations of narrowly endemic habitat specialists. PeerJ 5, e3632–e3632. https://doi.org/10.7717/peerj.3632 (2017).Article 

    Google Scholar 
    Ancillotto, L., Mori, E., Bosso, L., Agnelli, P. & Russo, D. The Balkan long-eared bat (Plecotus kolombatovici) occurs in Italy—First confirmed record and potential distribution. Mamm. Biol. 96, 61–67. https://doi.org/10.1016/j.mambio.2019.03.014 (2019).
    Article 

    Google Scholar 
    Imtiyaz, B. B., Sweta, P. D., Prakash, K. K. Threats to marine biodiversity. Mar. Biodivers.: Present Status Prospects (2011).Robinson, N. M., Nelson, W. A., Costello, M. J., Sutherland, J. E. & Lundquist, C. J. A systematic review of marine-based species distribution models (SDMs) with recommendations for best practice. Front. Mar. Sci. 4, 421 (2017).Article 

    Google Scholar 
    Fabri-Ruiz, S., Danis, B., David, B. & Saucède, T. Can we generate robust species distribution models at the scale of the Southern Ocean?. Divers. Distrib. 25, 21–37. https://doi.org/10.1111/ddi.12835 (2019).Article 

    Google Scholar 
    Maxwell, D. L., Stelzenmüller, V., Eastwood, P. D. & Rogers, S. I. Modelling the spatial distribution of plaice (Pleuronectes platessa), sole (Solea solea) and thornback ray (Raja clavata) in UK waters for marine management and planning. J. Sea Res. 61, 258–267. https://doi.org/10.1016/j.seares.2008.11.008 (2009).Article 
    ADS 

    Google Scholar 
    Marshall, C. E., Glegg, G. A. & Howell, K. L. Species distribution modelling to support marine conservation planning: The next steps. Mar. Policy 45, 330–332. https://doi.org/10.1016/j.marpol.2013.09.003 (2014).Article 

    Google Scholar 
    GBIF. GBIF Occurrence Download https://doi.org/10.15468/dl.khpu28. GBIF (2021).Spalding, M. D. et al. Marine ecoregions of the world: A bioregionalization of coastal and shelf areas. Bioscience 57, 573–583. https://doi.org/10.1641/B570707 (2007).Article 

    Google Scholar 
    Basher, Z., Bowden, D. A. & Costello, M. J. Global marine environment datasets (GMED). World Wide Web Electron. Publ. 14, 1 (2018).
    Google Scholar 
    Barnes, D. Ecology of subtropical hermit crabs in SW Madagascar: short-range migrations. Mar. Biol. 142, 549–557. https://doi.org/10.1007/s00227-002-0968-5 (2003).Article 

    Google Scholar 
    Naimullah, M. et al. Association of environmental factors in the Taiwan Strait with distributions and habitat characteristics of three swimming crabs. Remote Sens. 12, 1. https://doi.org/10.3390/rs12142231 (2020).Article 

    Google Scholar 
    Malvé, M. E., Rivadeneira, M. M. & Gordillo, S. Northward range expansion of the European green crab Carcinus maenas in the SW Atlantic: a synthesis after ~20 years of invasion history. bioRxiv, 2020.2011.2004.368761, doi:https://doi.org/10.1101/2020.11.04.368761 (2020).Merow, C., Smith, M. J. & Silander, J. A. Jr. A practical guide to MaxEnt for modeling species’ distributions: what it does, and why inputs and settings matter. Ecography 36, 1058–1069. https://doi.org/10.1111/j.1600-0587.2013.07872.x (2013).Article 

    Google Scholar 
    Naimi, B. & Araújo, M. B. sdm: a reproducible and extensible R platform for species distribution modelling. Ecography 39, 368–375. https://doi.org/10.1111/ecog.01881 (2016).Article 

    Google Scholar 
    Team, R. C. R: A Language and Environment for Statistical Computing (2020).Fielding, A. H. & Bell, J. F. A review of methods for the assessment of prediction errors in conservation presence/absence models. Environ. Conserv. 24, 38–49. https://doi.org/10.1017/S0376892997000088 (1997).Article 

    Google Scholar 
    Swets John, A. Measuring the Accuracy of Diagnostic Systems. Science 240, 1285–1293. https://doi.org/10.1126/science.3287615 (1988).Article 
    ADS 
    MathSciNet 
    MATH 

    Google Scholar 
    Phillips, S. J., Anderson, R. P., Dudík, M., Schapire, R. E. & Blair, M. E. Opening the black box: an open-source release of Maxent. Ecography 40, 887–893. https://doi.org/10.1111/ecog.03049 (2017).Article 

    Google Scholar 
    Hijmans, R. J. raster: Geographic Data Analysis and Modeling. R package version 3.3–7 (2020).UNEP-WCMC and IUCN. Protected Planet: The World Database on Protected Areas (WDPA) and World Database on Other Effective Area-based Conservation Measures (WD-OECM). UNEP-WCMC and IUCN (2021). More

  • in

    Improving access to aquatic foods

    Bennett, A. et al. Nat. Food https://doi.org/10.1038/s43016-022-00642-4 (2022).Article 

    Google Scholar 
    Simmance, F. A. et al. Nat. Commun. 3, 174 (2022).
    Google Scholar 
    Kolding, J., van Zwieten, P., Martin, F., Funge-Smith, S. & Poulain, F. Freshwater Small Pelagic Fish and Their Fisheries in the Major African Lakes and Reservoirs in Relation to Food Security and Nutrition (Food and Agriculture Organization of the United Nations, 2019).Pradhan, S. K., Nayak, P. K. & Armitage, D. Curr. Res. Environ. Sustain. 4, 100128 (2022).Article 

    Google Scholar 
    Byrd, K. A., Pincus, L., Pasqualino, M. M., Muzofa, F. & Cole, S. M. Matern. Child Nutr. 17, e13192 (2021).Article 

    Google Scholar 
    Chiwaula, L. S., Chirwa, G. C., Binauli, L. S., Banda, J. & Nagoli, J. Agric. Food Econ. 6, 1–15 (2018).Article 

    Google Scholar 
    Cole, S. M. et al. Ecol. Soc. 23, 18 (2018).Article 

    Google Scholar 
    Manyungwa, C. L., Hara, M. M. & Chimatiro, S. K. Marit. Stud. 18, 275–285 (2019).Article 

    Google Scholar 
    Coates, J. et al. Food Policy 81, 82–94 (2018).Article 

    Google Scholar 
    Stevens, G. A. et al. Lancet Glob. Health 10, e1590–e1599 (2022).Article 

    Google Scholar 
    Hicks, C. C. et al. Nat. Food 3, 851–861 (2022).Article 

    Google Scholar  More

  • in

    A signal-like role for floral humidity in a nocturnal pollination system

    Kulahci, I. G., Dornhaus, A. & Papaj, D. R. Multimodal signals enhance decision making in foraging bumble-bees. Proc. Biol. Sci. 275, 797–802 (2008).
    Google Scholar 
    Goldshtein, A. et al. Reinforcement learning enables resource partitioning in foraging bats. Curr. Biol. 30, 4096–4102.e4096 (2020).CAS 

    Google Scholar 
    Skogen, K. A., Overson, R. P., Hilpman, E. T. & Fant, J. B. Hawkmoth pollination facilitates long-distance pollen dispersal and reduces isolation across a gradient of land-use change. Ann. Mo. Bot. Gard. 104, 495–511 (2019). 417.
    Google Scholar 
    Deng, J.-Y., van Noort, S., Compton, S. G., Chen, Y. & Greeff, J. M. Conservation implications of fine scale population genetic structure of Ficus species in South African forests. Ecol. Manag. 474, 118387 (2020).
    Google Scholar 
    Galizia, C. G. et al. Relationship of visual and olfactory signal parameters in a food-deceptive flower mimicry system. Behav. Ecol. 16, 159–168 (2004).
    Google Scholar 
    Gibernau, M., HossaertMcKey, M., Frey, J. & Kjellberg, F. Are olfactory signals sufficient to attract fig pollinators. Ecoscience 5, 306–311 (1998).
    Google Scholar 
    Kapustjansky, A., Chittka, L. & Spaethe, J. Bees use three-dimensional information to improve target detection. Naturwissenschaften 97, 229–233 (2010).ADS 
    CAS 

    Google Scholar 
    Hempel de Ibarra, N., Langridge, K. V. & Vorobyev, M. More than colour attraction: behavioural functions of flower patterns. Curr. Opin. Insect Sci. 12, 64–70 (2015).
    Google Scholar 
    Boff, S., Henrique, J. A., Friedel, A. & Raizer, J. Disentangling the path of pollinator attraction in temporarily colored flowers. Int. J. Trop. Insect Sci. 41, 1305–1311 (2021).
    Google Scholar 
    Leonard, A. S. & Papaj, D. R. ‘X’ marks the spot: the possible benefits of nectar guides to bees and plants. Funct. Ecol. 25, 1293–1301 (2011).
    Google Scholar 
    Dobson, H. E. M. & Bergström, G. The ecology and evolution of pollen odors. Plant Syst. Evol. 222, 63–87 (2000).CAS 

    Google Scholar 
    Raguso, R. A. Why are some floral nectars scented? Ecology 85, 1486–1494 (2004).
    Google Scholar 
    Corbet, S. A., Kerslake, C. J. C., Brown, D. & Morland, N. E. Can bees select nectar-rich flowers in a patch. J. Apic. Res. 23, 234–242 (1984).
    Google Scholar 
    Policha, T. et al. Disentangling visual and olfactory signals in mushroom-mimicking Dracula orchids using realistic three-dimensional printed flowers. N. Phytol. 210, 1058–1071 (2016).CAS 

    Google Scholar 
    Stout, J. C., Goulson, D. & Allen, J. A. Repellent scent-marking of flowers by a guild of foraging bumblebees (Bombus spp.). Behav. Ecol. Sociobiol. 43, 317–326 (1998).
    Google Scholar 
    Howell, A. D. & Alarcón, R. Osmia bees (Hymenoptera: Megachilidae) can detect nectar-rewarding flowers using olfactory cues. Anim. Behav. 74, 199–205 (2007).von Arx, M. Floral humidity and other indicators of energy rewards in pollination biology. Commun. Integr. Biol. 6, e22750–e22750 (2013).
    Google Scholar 
    Goyret, J. The breath of a flower: CO2 adds another channel-and then some-to plant-pollinator interactions. Commun. Integr. Biol. 1, 66–68 (2008).CAS 

    Google Scholar 
    Bradbury, J. W. & Vehrencamp, S. L. Principles of Animal Communication 2nd edn (Sinauer Associates, 2011).McMeniman, C. J., Corfas, R. A., Matthews, B. J., Ritchie, S. A. & Vosshall, L. B. Multimodal integration of carbon dioxide and other sensory cues drives mosquito attraction to humans. Cell 156, 1060–1071 (2014).CAS 

    Google Scholar 
    Smith, J. M. & Harper, D. Animal Signals (Oxford Univ. Press, 2003).Smith, M. J. & Harper, D. G. C. Animal signals: models and terminology. J. Theor. Biol. 177, 305–311 (1995).ADS 

    Google Scholar 
    Laidre, M. E. & Johnstone, R. A. Animal signals. Curr. Biol. 23, R829–R833 (2013).CAS 

    Google Scholar 
    Smith, J. M. Must reliable signals always be costly? Anim. Behav. 47, 1115–1120 (1994).
    Google Scholar 
    Guerenstein, P. G., A.Yepez, E., van Haren, J., Williams, D. G. & Hildebrand, J. G. Floral CO2 emission may indicate food abundance to nectar-feeding moths. Naturwissenschaften 91, 329–333 (2004).ADS 
    CAS 

    Google Scholar 
    Goyret, J., Markwell, P. M. & Raguso, R. A. Context- and scale-dependent effects of floral CO2 on nectar foraging by Manduca sexta. Proc. Natl Acad. Sci. USA 105, 4565–4570 (2008).ADS 
    CAS 

    Google Scholar 
    Thom, C., Guerenstein, P. G., Mechaber, W. L. & Hildebrand, J. G. Floral CO2 reveals flower profitability to moths. J. Chem. Ecol. 30, 1285–1288 (2004).CAS 

    Google Scholar 
    Gilbert, F. S., Haines, N. & Dickson, K. Empty flowers. Funct. Ecol. 5, 29–39 (1991).
    Google Scholar 
    von Arx, M., Goyret, J., Davidowitz, G. & Raguso, R. A. Floral humidity as a reliable sensory cue for profitability assessment by nectar-foraging hawkmoths. Proc. Natl Acad. Sci. USA 109, 9471–9476 (2012).ADS 

    Google Scholar 
    Harrap, M. J. M., Hempel de Ibarra, N., Knowles, H. D., Whitney, H. M. & Rands, S. A. Floral humidity in flowering plants: A preliminary survey. Front. Plant Sci. https://doi.org/10.3389/fpls.2020.00249 (2020).Harrap, M. J. M. & Rands, S. A. The role of petal transpiration in floral humidity generation. Planta 255, 78 (2022).CAS 

    Google Scholar 
    Harrap, M. J. M., Hempel de Ibarra, N., Knowles, H. D., Whitney, H. M. & Rands, S. A. Bumblebees can detect floral humidity. J. Exp. Biol. https://doi.org/10.1242/jeb.240861 (2021).Hebets, E. A. & Papaj, D. R. Complex signal function: developing a framework of testable hypotheses. Behav. Ecol. Sociobiol. 57, 197–214 (2005).
    Google Scholar 
    Bronstein, J. L., Huxman, T., Horvath, B., Farabee, M. & Davidowitz, G. Reproductive biology of Datura wrightii: the benefits of a herbivorous pollinator. Ann. Bot. 103, 1435–1443 (2009).
    Google Scholar 
    Johnson, C. A. et al. Coevolutionary transitions from antagonism to mutualism explained by the co-opted antagonist hypothesis. Nat. Commun. https://doi.org/10.1038/s41467-021-23177-x (2021).Clark, C. J. The role of power versus energy in courtship: what is the ‘energetic cost’ of a courtship display? Anim. Behav. 84, 269–277 (2012).
    Google Scholar 
    Willmott, A. P. & Ellington, C. P. The mechanics of flight in the hawkmoth Manduca sexta. I. Kinematics of hovering and forward flight. J. Exp. Biol. 200, 2705–2722 (1997).CAS 

    Google Scholar 
    Shields, V. D. C. & Hildebrand, J. G. Fine structure of antennal sensilla of the female sphinx moth, Manduca sexta (Lepidoptera: Sphingidae). II. Auriculate, coeloconic, and styliform complex sensilla. Can. J. Zool. 77, 302–313 (1999).
    Google Scholar 
    Lee, J. K. & Strausfeld, N. J. Structure, distribution and number of surface sensilla and their receptor cells on the olfactory appendage of the male moth Manduca sexta. J. Neurocytol. 19, 519–538 (1990).CAS 

    Google Scholar 
    Shields, V. D. & Hildebrand, J. G. Recent advances in insect olfaction, specifically regarding the morphology and sensory physiology of antennal sensilla of the female sphinx moth Manduca sexta. Microsc. Res. Tech. 55, 307–329 (2001).CAS 

    Google Scholar 
    Tichy, H. & Loftus, R. Hygroreceptors in insects and a spider: Humidity transduction models. Naturwissenschaften 83, 255–263 (1996).ADS 
    CAS 

    Google Scholar 
    Ahrens, M., Huang, K.-H., Narayan, S., Mensh, B. & Engert, F. Two-photon calcium imaging during fictive navigation in virtual environments. Front. Neural Circuits https://doi.org/10.3389/fncir.2013.00104 (2013).Lacher, V. Elektrophysiologische untersuchungen an einzelnen rezeptoren für geruch, kohlendioxyd, luftfeuchtigkeit und tempratur auf den antennen der arbeitsbiene und der drohne (Apis mellifica L.). Z. f.ür. Vgl. Physiologie 48, 587–623 (1964).
    Google Scholar 
    Waldow, U. Elektrophysiologische untersuchungen an feuchte-, trocken- und kälterezeptoren auf der antenne der wanderheuschrecke Locusta. Z. f.ür. Vgl. Physiologie 69, 249–283 (1970).
    Google Scholar 
    Yokohari, F. & Tateda, H. Moist and dry hygroreceptors for relative humidity of the cockroach, Periplaneta americana L. J. Comp. Physiol. 106, 137–152 (1976).
    Google Scholar 
    Tichy, H. Low rates of change enhance effect of humidity on the activity of insect hygroreceptors. J. Comp. Physiol. A Neuroethol. Sens Neural Behav. Physiol. 189, 175–179 (2003).CAS 

    Google Scholar 
    Tichy, H., Hellwig, M. & Kallina, W. Revisiting theories of humidity transduction: a focus on electrophysiological data. Front. Physiol. 8, 650 (2017).
    Google Scholar 
    Tichy, H. & Kallina, W. Insect hygroreceptor responses to continuous changes in humidity and air pressure. J. Neurophysiol. 103, 3274–3286 (2010).CAS 

    Google Scholar 
    Wolfin, M. S., Raguso, R. A., Davidowitz, G. & Goyret, J. Context dependency of in-flight responses by Manduca sexta moths to ambient differences in relative humidity. J. Exp. Biol. https://doi.org/10.1242/jeb.177774 (2018).Smith, G., Kim, C. & Raguso, R. A. Pollen accumulation on hawkmoths varies substantially among moth-pollinated flowers. Preprint at bioRxiv https://doi.org/10.1101/2022.07.15.500245 (2022).Haverkamp, A., Bing, J., Badeke, E., Hansson, B. S. & Knaden, M. Innate olfactory preferences for flowers matching proboscis length ensure optimal energy gain in a hawkmoth. Nat. Commun. 7, 11644 (2016).ADS 
    CAS 

    Google Scholar 
    Harrison, A. S. & Rands, S. A. The ability of bumblebees Bombus terrestris (hymenoptera: Apidae) to detect floral humidity is dependent upon environmental humidity. Environ. Entomol. 51, 1010–1019 (2022).
    Google Scholar 
    Kelber, A. What a hawkmoth remembers after hibernation depends on innate preferences and conditioning situation. Behav. Ecol. 21, 1093–1097 (2010).
    Google Scholar 
    Riffell, J. A. et al. Flower discrimination by pollinators in a dynamic chemical environment. Science 344, 1515–1518 (2014).ADS 
    CAS 

    Google Scholar 
    Schellenberg, R. The trouble with humidity: the hidden challenge of RH calibration. Cal. Lab. 9, 40–42 (2002).
    Google Scholar 
    Roddy, A. B., Brodersen, C. R. & Dawson, T. E. Hydraulic conductance and the maintenance of water balance in flowers. Plant Cell Environ. 39, 2123–2132 (2016).CAS 

    Google Scholar 
    Sane, S. P. & Jacobson, N. P. Induced airflow in flying insects. II. Measurement of induced flow. J. Exp. Biol. 209, 43–56 (2006).
    Google Scholar 
    Daly, K. C., Kalwar, F., Hatfield, M., Staudacher, E. & Bradley, S. P. Odor detection in Manduca sexta is optimized when odor stimuli are pulsed at a frequency matching the wing beat during flight. PLoS ONE 8, e81863 (2013).ADS 

    Google Scholar 
    Yokohari, F. Hygroreceptor mechanism in the antenna of the cockroach. Periplaneta. J. Comp. Physiol. 124, 153 (1978).
    Google Scholar 
    Loftus, R. Temperature-dependent dry receptor on antenna of Periplaneta. Tonic response. J. Comp. Physiol. 111, 153–170 (1976).
    Google Scholar 
    Tichy, H. & Kallina, W. Sensitivity of honeybee hygroreceptors to slow humidity changes and temporal humidity variation detected in high resolution by mobile measurements. PLoS ONE 9, e99032 (2014).ADS 

    Google Scholar 
    Galen, C., Sherry, R. A. & Carroll, A. B. Are flowers physiological sinks or faucets? Costs and correlates of water use by flowers of Polemonium viscosum. Oecologia 118, 461–470 (1999).ADS 

    Google Scholar 
    Elle, E., van Dam, N. M. & Hare, J. D. Cost of glandular trichomes, a “resistance” character in Datura wrightii regel (solanaceae). Evolution 53, 22–35 (1999).
    Google Scholar 
    Elle, E. & Hare, J. D. Environmentally induced variation in floral traits affects the mating system in Datura wrightii. Funct. Ecol. 16, 79–88 (2002).
    Google Scholar 
    Marler, C. A. & Ryan, M. J. Energetic constraints and steroid hormone correlates of male calling behaviour in the túngara frog. J. Zool. 240, 397–409 (1996).
    Google Scholar 
    Bernal, X. E., Rand, A. S. & Ryan, M. J. Acoustic preferences and localization performance of blood-sucking flies (Corethrella Coquillett) to túngara frog calls. Behav. Ecol. 17, 709–715 (2006).
    Google Scholar 
    Raguso, R. A. Flowers as sensory billboards: progress towards an integrated understanding of floral advertisement. Curr. Opin. Plant Biol. 7, 434–440 (2004).
    Google Scholar 
    Peach, D. A. H., Gries, R., Zhai, H., Young, N. & Gries, G. Multimodal floral cues guide mosquitoes to tansy inflorescences. Sci. Rep. 9, 3908 (2019).ADS 

    Google Scholar 
    Riffell, J. A. & Alarcón, R. Multimodal floral signals and moth foraging decisions. PLoS ONE 8, e72809 (2013).ADS 
    CAS 

    Google Scholar 
    van der Kooi, C. J., Kevan, P. G. & Koski, M. H. The thermal ecology of flowers. Ann. Bot. 124, 343–353 (2019).
    Google Scholar 
    Terry, L. I., Roemer, R. B., Walter, G. H., Booth, D. & Lee, K. P. Thrips’ responses to thermogenic associated signals in a cycad pollination system: the interplay of temperature, light, humidity and cone volatiles. Funct. Ecol. 28, 857–867 (2014).
    Google Scholar 
    Bronstein, J. L., Alarcón, R. & Geber, M. The evolution of plant–insect mutualisms. N. Phytol. 172, 412–428 (2006).
    Google Scholar 
    Schaefer, H. M. & Ruxton, G. D. Deception in plants: mimicry or perceptual exploitation. Trends Ecol. Evol. 24, 676–685 (2009).
    Google Scholar 
    Franchi, G. G., Nepi, M. & Pacini, E. Is flower/corolla closure linked to decrease in viability of desiccation-sensitive pollen? Facts and hypotheses: a review of current literature with the support of some new experimental data. Plant Syst. Evol. 300, 577–584 (2014).
    Google Scholar 
    Safavian, D. et al. High humidity partially rescues the Arabidopsis thaliana exo70A1 stigmatic defect for accepting compatible pollen. Plant Reprod. 27, 121–127 (2014).CAS 

    Google Scholar 
    Shivanna, K. R. & Cresti, M. Effects of high humidity and temperature stress on pollen membrane integrity and pollen vigour in Nicotiana tabacum. Sex. Plant Reprod. 2, 137–141 (1989).
    Google Scholar 
    Richman, S. K. et al. The sensory and cognitive ecology of nectar robbing. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2021.698137 (2021).Raguso, R. A. et al. Trumpet flowers of the Sonoran Desert: floral biology of Peniocereus Cacti and Sacred Datura. Int. J. Plant Sci. 164, 877–892 (2003).CAS 

    Google Scholar 
    Carazo, P. & Font, E. ‘Communication breakdown’: the evolution of signal unreliability and deception. Anim. Behav. 87, 17–22 (2014).
    Google Scholar 
    Schemske, D. W. Evolution of floral display in the orchid Brassavola nodosa. Evolution 34, 489–493 (1980).
    Google Scholar 
    Haber, W. A. Pollination by deceit in a mass-flowering tropical tree Plumeria rubra L. (apocynaceae). Biotropica 16, 269–275 (1984).
    Google Scholar 
    Brandenburg, A., Kuhlemeier, C. & Bshary, R. Hawkmoth pollinators decrease seed set of a low-nectar Petunia axillaris line through reduced probing time. Curr. Biol. 22, 1635–1639 (2012).CAS 

    Google Scholar 
    Bye, R. & Sosa, V. Molecular phylogeny of the jimsonweed genus Datura (solanaceae). Syst. Bot. 38, 818–829 (2013).
    Google Scholar 
    Kariñho-Betancourt, E., Agrawal, A. A., Halitschke, R. & Núñez-Farfán, J. Phylogenetic correlations among chemical and physical plant defenses change with ontogeny. N. Phytol. 206, 796–806 (2015).
    Google Scholar 
    Kawahara, A. Y. et al. Evolution of Manduca sexta hornworms and relatives: biogeographical analysis reveals an ancestral diversification in Central America. Mol. Phylogenet. Evol. 68, 381–386 (2013).
    Google Scholar 
    Contreras, H. L. et al. The effect of ambient humidity on the foraging behavior of the hawkmoth Manduca sexta. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 199, 1053–1063 (2013).
    Google Scholar 
    Cardoso, J. C. F., Gonzaga, M. O., Cavalleri, A., Maruyama, P. K. & Alves-Silva, E. The role of floral structure and biotic factors in determining the occurrence of florivorous thrips in a dystilous shrub. Arthropod-Plant Interact. 10, 477–484 (2016).
    Google Scholar 
    Nicolson, S. W. Sweet solutions: nectar chemistry and quality. Philos. Trans. R. Soc. Lond. B Biol. Sci. 377, 20210163 (2022).CAS 

    Google Scholar 
    Pellmyr, O. & Thien, L. B. Insect reproduction and floral fragrances: keys to the evolution of the Angiosperms. Taxon 35, 76–85 (1986).
    Google Scholar 
    Enjin, A. et al. Humidity sensing in Drosophila. Curr. Biol. 26, 1352–1358 (2016).CAS 

    Google Scholar 
    Knecht, Z. A. et al. Distinct combinations of variant ionotropic glutamate receptors mediate thermosensation and hygrosensation in Drosophila. eLife 5, e17879 (2016).
    Google Scholar 
    Knecht, Z. A. et al. Ionotropic receptor-dependent moist and dry cells control hygrosensation in Drosophila. eLife 6, e26654 (2017).
    Google Scholar 
    Croset, V. et al. Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genet. 6, e1001064–e1001064 (2010).
    Google Scholar 
    Dahake, A. et al. MATLAB codes: a signal-like role for floral humidity in a nocturnal pollination system. Zenodo https://doi.org/10.5281/zenodo.7320037 (2022).Pereira, T. D. et al. Fast animal pose estimation using deep neural networks. Nat. Methods 16, 117–125 (2019).CAS 

    Google Scholar 
    Nilsson, S. R. et al. Simple behavioral analysis (SimBA) – an open source toolkit for computer classification of complex social behaviors in experimental animals. Preprint at bioRxiv https://doi.org/10.1101/2020.04.19.049452 (2020).Casey, T. M. Flight energetics of sphinx moths: power input during hovering flight. J. Exp. Biol. 64, 529–543 (1976).CAS 

    Google Scholar 
    Riffell, J. A. et al. Behavioral consequences of innate preferences and olfactory learning in hawkmoth-flower interactions. Proc. Natl Acad. Sci. USA 105, 3404–3409 (2008).ADS 
    CAS 

    Google Scholar 
    Lott, G. K., Johnson, B. R., Bonow, R. H., Land, B. R. & Hoy, R. R. g-PRIME: a free, windows based data acquisition and event analysis software package for physiology in classrooms and research labs. J. Undergrad. Neurosci. Educ. 8, A50–A54 (2009).
    Google Scholar 
    Chaure, F. J., Rey, H. G. & Quiroga, R. Q. A novel and fully automatic spike-sorting implementation with variable number of features. J. Neurophysiol. 120, 1859–1871 (2018).CAS 

    Google Scholar 
    Tichy, H. Humidity-dependent cold cells on the antenna of the stick insect. J. Neurophysiol. 97, 3851–3858 (2007).
    Google Scholar 
    Campbell, R. raacampbell/shadedErrorBar. https://github.com/raacampbell/shadedErrorBar (2022).Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. https://doi.org/10.18637/jss.v067.i01 (2015).Broadhead, G. T. & Raguso, R. A. Associative learning of non-sugar nectar components: amino acids modify nectar preference in a hawkmoth. J. Exp. Biol. https://doi.org/10.1242/jeb.234633 (2021). More

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    Anthrax hotspot mapping in Kenya support establishing a sustainable two-phase elimination program targeting less than 6% of the country landmass

    Data sourcesThis study builds on two datasets; 666 livestock anthrax outbreaks collected over 60 years (1957–2017) by the Kenya Directorate of Veterinary Services (KDVS), and 13 reported anthrax outbreaks we investigated between 2017 and 201811,13. These datasets were combined with data from targeted active anthrax surveillance we conducted in 2019–2020 (see below) to define anthrax suitable areas in Kenya, including hotspots, and subsequently assessed effectiveness of livestock vaccination as a control strategy.Targeted active surveillance-collected anthrax data, 2019–2020Active anthrax surveillance was conducted for 12 months between 2019 and 2020 in randomly selected areas to ensure representation of all AEZs of the country. AEZs are land units defined based on the patterns of soil, landforms and climatic characteristics. Kenya has seven AEZs that include agro-alpine, high potential, medium potential, semi-arid, arid, very-arid and desert. In 2013, Kenya devolved governance into 47 semi-autonomous counties that are subdivided into 290 subcounties which are in turn divided into 1450 administrative wards, the smallest administrative units in the country. Using a geographic map that condensed Kenya into five AEZs; agro-alpine, high potential, medium potential, semi-arid, and arid/very arid zones, we randomly selected 4 administrative sub-counties from each AEZ (N = 20). To increase geographic spread of the study and enhance detection of anthrax outbreaks, we surveilled the larger administrative county (consisting of 20 to 45 administrative wards) where the randomly selected sub-counties were located. As shown in Fig. S1, we ultimately carried out the active anthrax surveillance in 18 counties, containing 523 administrative wards, the latter being used for measuring spatial association (see below).We conducted the surveillance between April 2019 and June 2020, through 523 animal health practitioners (AHPs), one in each ward, after intensive training to identify anthrax using a standard case definition, and to collect and electronically transmit the data weekly using telephone-based short messaging system (SMS) to a central server hosted by KDVS. Regarding case definition, any livestock death classified as anthrax through clinical or laboratory diagnosis was considered an anthrax event. Using standard guidelines issued by the KDVS, a clinical diagnosis was made by the AHPs across the country as an acute cattle, sheep or goat disease characterized by sudden death with or without bleeding from natural orifices, accompanied by absence of rigor mortis. Further, if the carcass was accidentally opened, failure of blood to clot and/or the presence of splenomegaly were included. In pigs, symptoms included swelling of the face and neck with oedema. A laboratory confirmed anthrax was diagnosed using Gram and methylene blue stains followed by identification of the capsule and typical rod-shaped B. anthracis in clinical specimens that the AHPs submitted to the central or regional veterinary investigation laboratories in Kenya. One case of anthrax in either species was considered an outbreak.During the surveillance, the programmed server sent prompting texts directly to the AHPs’ cell phones every Friday of each week for the 52 weeks. The AHPs interacted with the platform by responding to prompting questions sent via SMS to their telephones. Data were securely stored in an online encrypted platform which was subsequently downloaded into Ms Excel for analysis. This surveillance detected 119 anthrax outbreaks, whose partial data were used to model effects of climate change on future anthrax distribution in Kenya14. Here, we integrated these active surveillance data with other datasets to conduct detailed ENM and kernel-smoothed density mapping with a goal of refining suitable anthrax areas including crystalizing hotspots in the country.Anthrax outbreak incidence per livestock population by countyWe knew the total number of livestock per county and wards by species for the active surveillance period. The counties represented the level of disease management including vaccine distribution while the wards within counties represented the modeling unit for targeting control. Therefore, we estimated the outbreak incidence as the total number of outbreaks per livestock species per 100,000 head of that species.Ecological niche modeling and validationWe used boosted regression tree (BRT) algorithm as previously published13. In those studies, we estimated the geographic distribution of anthrax in southern Kenya using 69 spatially unique outbreak points (thinned from the 86 outbreaks in the records) and 18 environmental variables resampled to 250 m resolution. In this study, the final experiments were run with a learning rate (lr) = 0.001, bagging fraction (br) = 5, and maximum tree = 2500. We then mapped anthrax suitability as the mean output of the 100 experiments and the lower 2.5% and upper 97.5% mapped as confidence intervals. We determined variable contribution and derived partial dependence as previously described13. As BRTs are a random walk and each experiment randomly resamples training and test data, it was necessary to repeat those outputs along with the map predictions.Here, our goal was to evaluate the BRT models built with records data from 2011 to 2017 data and use the predict function to calculate model accuracy metrics using the 2017–2020 outbreaks as presence points and the sub-counties reporting zero outbreaks during the 2019–2020 active surveillance period as absence points. The model of southern Kenya was projected onto all of Kenya using climate variables clipped to the whole of Kenya. We tested the BRT models in two ways; first, evaluating 2011–2017 data models with holdout data using a random resampling and multi-modeling approach. Here, we report the area under curve (AUC) for each of the original training/testing split into the 69 historical points and the 2017–2020 data serving as independent data, the latter representing true model validation. Second, to determine the total percentage of surveillance data predicted and map areas of anthrax suitability to compare with kernel density estimates (see below), we produced a dichotomized map using the Youden index cutoff17 following Otieno et al.14.Outbreak concentrations from kernel density estimation (KDE)To describe the spatial concentration of reported outbreaks, we calculated descriptive spatial statistics, including the spatial mean, standard distance, and standard deviational ellipse of outbreak locations from the prospective surveillance dataset following Blackburn et al.18 These spatial statistics help to differentiate the geographic focus (spatial mean) and dispersion of outbreak reports from year to year and across the sampling period. We then conducted kernel density estimation (KDE) to visualize the concentration of anthrax outbreaks per square kilometer per year and across the study period18. We used the spatstat package for all KDE analyses using the quadratic kernel function19:$$fleft( x right) = frac{1}{{nh^{2} }} mathop sum limits_{i = 1}^{n} Kleft( {frac{{x – X_{i} }}{h}} right)$$where h is the bandwidth, x-Xi is the distance to each anthrax outbreak i. Finally, K is the quadratic kernel function, defined as:$$Kleft( x right) = frac{3}{4}left( {1 – x^{2} } right), left| x right| le 1$$$$Kleft( x right) = 0,x > 1$$This function was employed to estimate anthrax outbreak concentration across space using each outbreak weighted as one. We calculated the bandwidth (kernel) using hopt that uses the sample size (number of outbreaks) and the standard distance to estimate bandwidth. Finally, we estimated bandwidth for each year and then averaged them to apply the same fixed bandwidth for each year under study in Q-GIS version 3.1.8. The resulting outputs were map surfaces representing the spatial concentrations of outbreaks across the country per 1 km2 for each study year and all study years combined. For this study, we used the cutoff criteria of Nelson and Boots19 to identify outbreak hotspots as areas with density values in the upper 25%, 10%, and 5% of outbreak concentrations. The analyses identified these areas by year (2017–2020) and for all surveillance years combined.Local spatial clustering at the ward levelAnthrax outbreak incidence per livestock speciesThe ENM and KDE-derived maps provide a first estimate of potential risk and outbreak concentration, respectively. We were also interested in estimating anthrax outbreak intensity relative to livestock populations at a local level. For the active surveillance period, we knew the total number of outbreaks per ward (the smallest administrative spatial unit) by livestock species. For this two-year period, we estimated the ward-level outbreak incidence as the total number of outbreaks per livestock species per 10,000 head of that species. To estimate livestock population per ward, we extracted the values in the raster file of the areal weighted gridded livestock of the world data using the zonal statistic routine in Q-GIS version 3.1.8, into the polygon consisting of all pixels per ward as the total population19,20. We calculated outbreak incidence as the number of outbreaks per ward cattle population per 10,000 cattle for each administrative ward. We limited this analysis to those 18 counties participating in the active surveillance study (Fig. S1), as we could appropriately assume any ward with no reports was a ‘true zero’ for the estimation. Given that most reported outbreaks were in domestic cattle (see results below), we here report those results involving cattle alone. Given the overall high number of wards and the high number of wards without outbreaks, we performed the empirical Bayes smoothing and spatial Bayes smoothing routines in GeoDa version 1.12.1.161 to reduce the variance in anthrax incidence estimates20,21. To evaluate smoothing routine performance, we box plotted rates per ward and selected the method with the greatest reduction in outliers21. Smoothed rates were mapped as choropleth map in Q-GIS version 3.1.8 using the four equal area bins.Spatial cluster analysisWe used Local Moran’s I16 to test for spatial cluster of livestock anthrax in cattle using the smoothed outbreak incidence estimates. The Local Moran’s I statistic tests whether individual wards are part of spatial cluster, like incidence estimates surrounded by similar estimate (high-high or low-low) or spatial outliers where wards with significantly high or low estimates are surrounded by dissimilar values (high-low or low–high). The local Moran’s I is written as16:$$I_{i} = Z_{i} sum W_{ij} Z_{j}$$where Ii is the statistic for a ward i, Zi is the difference between the incidence at i and the mean anthrax incidence rate for all of wards in the study, Zj is the difference between anthrax risk at ward j and the mean for all wards. Wij is the weights matrix. In this study, the 1st order queen contiguity was employed. Here, Wij equals 1/n if a ward shared a boundary or vertex and 0 if not. For this study, Local Moran’s I was performed on the wards using 999 permutations and p = 0.05 using GeoDa version 1.12.1.161.Assessing effectiveness of cattle vaccination in burden hotspotsAs a first estimate of how we might scale up livestock anthrax vaccination efforts in Kenya, we slightly adjusted a simple published anthrax outbreak simulation model in a cattle population. For this study we applied an early mathematical approach of Funiss and Hahn22 to simulate anthrax at the ward level. While other recent models are available23,24, these are difficult to parameterize or require time series data we could not derive with the surveillance approach in this study. Like the more recent models, Funiss and Hahn22 assumed anthrax transmission was driven by cattle accessing spore-contaminated environments. Here the proportion of infected cattle each day depended on the population of susceptible animals in the population and probability of getting infected. This probability depends on environmental contamination (“a”), and a fraction of anthrax carcasses in the environment on a day (“f,”). Each day, the newly infected cattle are transferred to an incubation period vector, “d,” waiting to die following a probability “p”. In this model, all infected animals, “n,” die following the incubation periods given by the vector, “p”, in which pi is the probability of a cow dying i days after the infection. Following death, the cattle are transferred to a carcass state, providing a direct infection source to the susceptible cattle via environmental contamination. Environmental contamination “a,” is therefore defined as the number of spores ingested by an animal in a day. This environmental contamination depends on spores from carcasses and an assumed spore decay rate γ22.The complete set of difference equations with a daily time step is given by:$${text{S}}_{(t + 1)} = {text{S}}_{(t)} – {text{ S}}_{(t)} *left( {{1} – {text{e}}^{{ – left( {{text{a}}_{t} + gamma {text{f}}_{{{text{t}} + 1}} } right)}} } right)$$$${text{I}}_{(t + 1)} = {text{I}}_{(t)} + {text{ S}}_{(t)} *left( {{1} – {text{e}}^{{ – left( {{text{a}}_{{text{t}}} + gamma {text{f}}_{{{text{t}} + {1}}} } right)}} } right)$$where the expression (left( {{1} – {text{e}}^{{ – left( {{text{a}}_{t} + gamma {text{f}}_{{{text{t}} + 1}} } right)}} } right)) denotes the probability of an animal becoming infected and at + γft+1 is the mean number of spores ingested by a cow in a day. The equation for environmental contamination, a, is given by:$${text{a}}_{t + 1} {-}{text{a}}_{{text{t}}} = alpha {text{a}}_{{text{t}}} + beta {text{c}}_{{{text{t}} + {1}}}$$The newly infected animals die after a certain number of days. The distribution of incubation periods is given by the vector, p. On each day, the new cases are placed in a due-to-die vector, d, and when they die, they are subsequently moved down one step to fresh carcasses, ft. The fresh carcasses provide a direct source of infection to the susceptible cattle via the ‘fresh carcass term’, γ. These carcasses decay or are scavenged or disposed by man. The equation expressing the disseminating carcasses, c, is:$${text{C}}_{t + 1} – {text{c}}_{t} = {text{f}}_{t + 1} – delta {text{c}}_{t}$$The model parameters variables are provided in Table 1 and are similar to those used by Funiss and Hahn22 to generate a standard run. We ran the model for one year and extrapolated to cattle population in the identified hotspot wards.Table 1 Model parameters and variables.Full size table More

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    The China plant trait database version 2

    Site selection and sampling strategyField sites (Table 1) were selected to represent typical natural vegetation types showing little or no signs of disturbance. Although much of the natural vegetation of China has been altered by human activities, there are still extensive areas of natural vegetation. Access to these areas is facilitated by the existence of a number of ecological transects39,40, the ChinaFlux network (http://www.chinaflux.org) and the Chinese Ecosystem Research Network (http://www.cern.ac.cn/0index/index.asp).About half the sites in CPTDv1 used a stratified sampling approach and this approach was used at all of the new sites added in the CPTDv2. This sampling strategy involves sampling the dominant species within each vegetation stratum so as to be able to characterise trait values at community level18. Specifically, a total of 25 trees, 5 shrubs, 5 lianas or vines, and 5 understorey species (grasses, forbs) were sampled at each site. When there were less than 25 trees at a site, all of the tree species were sampled and additional examples from the other categories were included up to the maximum of 40 species. If there are more than the maximum sampling number in any one category, then the dominant (i.e. most common) representatives of each category were sampled. Sampled individuals of each species were mature, healthy plants. In principle, sun leaves (i.e. leaves in the canopy and fully exposed to sunlight) were sampled. For true shade-tolerant and understory species, the sampled individuals were those in well-lit environments and isolated to minimize interactions with other individuals.Nineteen sites from Xinjiang included in CPTDv1 used a simplified sampling strategy, where only canopy species were sampled. Sixteen sites from Xinjiang were particularly depauperate and thus only a limited number of species were sampled without consideration of abundance. These sites are retained in the database because they sample extremely arid location with α typically less than 0.25Species identification and taxonomic standardisationSampled plants were identified in the field by a taxonomist familiar with the local vegetation, most usually using a regional flora. Species names were subsequently standardised using the online version of the Flora of China (http://www.efloras.org/flora_page.aspx?flora_id=2). Where field-identified species were not accepted or included in the Flora of China, and thus could not be assigned unambiguously to an accepted taxonomic name, we cross-checked whether the species were listed in the Plant List (http://www.theplantlist.org/) (or alternative sources such as the Virtual Herbarium of China, Plants of the World Online or TROPICOS) in order to identify synonyms for these accepted names that were recognised by the Flora of China. In cases where we were unable to identify an accepted name consistent with the Flora of China, we retained the field-assigned name by default (Fig. 3). The decisions about taxonomy are described in the CPTDv2 table “Taxonomic Standardisation” (Table 2). The names assigned originally in the field and the accepted standardized names used in the database are given in the CPTDv2 table “Species Translations” (Table 3). When species were recognised in the Flora of China, we provide the Chinese translation of the species name. The written Chinese nomenclature system does not follow the Linnaean system, so this table of “Species Chinese Name” is designed to facilitate the use of the database by botanists in China (Table 4). There are no translations of names that are not recognized by the Flora of China and are used in the database by default.Fig. 3Flowchart showing the decision tree used to determine the names used in the China Plant Database (accepted names) and encapsulated in the Taxonomic Standardization table. ‘=1’ and ‘ >1’ indicate the number of Synonyms is equal or more than one.Full size imageDataset collection methodsPhotosynthetic pathwayInformation on photosynthetic pathway (Table 5) was obtained for each species from the literature. There are a large number of literature compilations on the photosynthetic pathway of Chinese plants (e.g.41,42,43,44,45,46. Where this information was not available from Chinese studies we used similar compilations from other regions of the world (e.g.47,48,49,50,51,52. Since C4 plants have much less carbon discrimination than C3 plants, the measurements on δ13C were also used as an indicator of the photosynthetic pathway53,54,55,56. δ13C value of –20‰ was applied as a threshold of C3 photosynthetic pathway distinction54. Information about photosynthetic pathway was not included for a species unless confirmed from the literature or δ13C measurements.Leaf physical and chemical traitsPhysical and chemical properties (Table 6) were measured on samples collected in the field following standard methods37. At least 10 g of leaves were collected for each species. Sunlit leaves of tree species were obtained with long-handled twig shears. The samples were subdivided for the measurement of specific leaf area, leaf dry matter content and the contents of carbon, nitrogen, phosphorus and potassium. Recorded values were the average of three replicates. Leaf area was determined by scanning five leaves (or more in the case of small leaves, to make up a total area ≥20 cm2 per species) with a laser scanner. Areas (Average LA) were measured using Photoshop on the scanned images. Leaf fresh weight was measured in the field. Dry weight was obtained after air drying for several days and then oven drying at 75 °C for 48 hours. Leaf dry matter content (LDMC) was expressed as leaf oven-dry weight divided by fresh weight. Specific leaf area (SLA) was then expressed as the ratio between leaf area and leaf dry mass. LMA is the inverse of SLA. Leaf carbon content (Cmass) was measured by the potassium dichromate volumetric method and leaf nitrogen content (Nmass) by the Micro-Kjeldahl method. Leaf phosphorus (Pmass) was analysed colorimetrically (Shimadzu UV-2550). Leaf potassium (Kmass) was measured by Flame Atomic Emission Spectrophotometry (PE 5100 PC). The area-based leaf chemical contents (Carea, Narea, Parea, Karea) were derived as a product of mass-based content and LMA. δ13C (d13C:12C) and δ15N (d15N:14N) were measured using the Isotope Ratio Mass Spectrometer (Thermo Fisher Scientific Inc., USA; Finnigan Corporation, San Jose, CA).Photosynthetic traitsSeveral different methods were used to characterise photosynthetic traits (Supplementary Table 1). Chlorophyll fluorescence measurements were made at the sites along Northeast China Transect. These measurements were recorded as the potential (Fv/Fm) and actual (QY) rates of photosynthetic electron transport. QY is correlated with photosynthetic rate, although it also includes the diversion of electrons to non-photosynthetic activities such as the elimination of reactive oxygen species57. Measurements of photosynthetic traits at most of the sites (about 68% of samples with photosynthetic measurements) were derived from leaf gas-exchange measurements in light-saturated conditions under either ambient or high CO2 levels, made with a portable infrared gas analyser (IRGA) system (LI-6400; Li-Cor Inc., Lincoln, NB, USA). Sunlit terminal branches from the upper canopy were collected and re-cut under water immediately prior to measurement. Measurements were made in the field with relative humidity and chamber block temperature close to that of the ambient air at the time of measurement, and a constant airflow rate (500 μmol s−1). The maximum capacity of carboxylation (Vcmax) and electron-transport (Jmax) were calculated from the light-saturated rate of net CO2 fixation at ambient and high CO2 level respectively using the one-point method for Vcmax58 and two-point method for Jmax59. Although it was indicated that applying one-point method could result in around 20% error in measuring photosynthetic capacity60, this time-saving method indeed allows much more samples to be measured in the field. For sites in CPTDv1, the Vcmax and Jmax values were made on a single specimen of each species at each site, due to the time-consuming nature of the measurement. For the newly collected sites in CPTDv2, for each species the Vcmax and Jmax were measured on three samples collected from three individual tress. The average values were recorded in the database. For Vcmax measurements, the CO2 level was set as the ambient atmospheric CO2 level, ranging from 380 ppm to 400 ppm. The leaves were exposed to a typical photosynthetic photon flux density (PPFD) of 1800 μmol m−2 s−1 with the light source. Pre-processing method was applied to determine the saturating PPFD for alpine plants, which goes up to 2000 μmol m−2 s−1 in the high elevation sites from Mountain Gonga. For Jmax measurements, the CO2 level was set as 1500 ppm or 2000 ppm to avoid any limitation on photosynthesis via carboxylation.There are a few cases (1 site from Cai, et al.61, and 8 sites from Zheng and Shangguan62, Zheng and Shangguan63), where field-measured ratio of leaf internal- to ambient-CO2 concentration (ci:ca) were not provided. In these cases, estimates of the ci:ca ratio were made from δ13C measurements using the method of64 to calculate isotopic discrimination (Δ) from δ13C (correcting for atmospheric δ13C, approximated as a function of time of collection and latitude), and the Ubierna and Farquhar65 method to calculate isotopic discrimination (Δ) from δ13C considering discrimination during stomatal diffusion and carboxylation. The R code for calculating Vcmax and Jcmax from original data was provided (seeing Code availability).Hydraulic traitsCPTDv2 contains information on four important hydraulic traits: specific sapwood conductivity, the sapwood to leaf area ratio (Huber value, vH), turgor loss point and wood density (Table 7). Hydraulic traits were measured on branches with a diameter wider than 7 mm, cut as close to the bifurcation point as possible to minimize any effect of measurement location on measured area. A section was taken from the part of the branch nearest to the bifurcation point, and the cross-sectional area of the xylem was measured at both ends of this section using digital calipers. Sapwood area was calculated as the average of these two measurements. All leaves attached to the branch were removed and dried at 70 °C for 72 hours before weighing. The total leaf area was obtained from dry mass and LMA. vH was calculated as the ratio of sapwood area and leaf area. The vH value recorded for each species at each site was the average of three measurements made on branches from different individuals.Five branches from at least three mature individuals of each species at each site were collected, wrapped in moist towels and sealed in black plastic bags, and then immediately transported to the laboratory. All the samples were re-cut under water, put into water and sealed in black plastic bags to rehydrate overnight. Sapwood-specific hydraulic conductivity, (KS) was measured using the method of Sperry, et al.66. Segments (10–15 cm length) were cut from the rehydrated branches and flushed using 20 mmol L−1 KCl solution for at least 30 minutes (to remove air from the vessels) until constant fluid dripped from the section. The segments were then placed under 0.005 MPa pressure to record the time (t) they took to transport a known water volume (W, m3). Length (L, m), sapwood area of both ends (S1 and S2, m2) and temperature (Tm, °C) were recorded. Sapwood-specific hydraulic conductivity at measurement temperature (KS,m, mol m−1 s−1 MPa−1) was calculated using Eq. (1). This was transformed to KS at mean maximum temperature during the growing season (KS,gt) and standard temperature (KS25) following Eqs. (2–3):$${K}_{S,m}={W,L{rho }_{w}/[0.005,t({S}_{1}+{S}_{2})/2]}(1000/,18)$$
    (1)
    $${K}_{S,t}={K}_{S,m}{eta }_{m}/{eta }_{t}$$
    (2)
    $$eta =1{0}^{-3}exp[A+B/,(C+T)]$$
    (3)
    where ηm and ηt (Pa s) are the water viscosity at measurement temperature and transformed temperature (i.e. mean maximum daytime temperature during the growing season and at a standard temperature of 25 °C), respectively, and ρw (kg m−3) is the density of water. The parameter values used in Eq. (3) were A = −3.719, B = 580 and C = −13867.A small part of each sapwood segment was used to measure wood density, the ratio of dry weight to volume of sapwood. After removal of bark and heartwood, the volume of sapwood was measured by displacement and the sapwood dry weight was obtained after drying at 70 °C for 72 hours to constant weight.The method described by Bartlett, et al.68 was used for the rapid determination of turgor loss point (Ψtlp). After rehydration overnight, discs were sampled using a 6-mm-diameter punch from mature, healthy leaves collected on each branch, avoiding major and minor veins. Leaf discs wrapped in foil were frozen in liquid nitrogen for at least 2 minutes and then punctured 20 times quickly with sharp-tipped tweezers. Five repeat experiments using leaves from multiple individuals were carried out for every species at each site. The osmotic potential (Ψosm) was measured with a VAPRO 5600 vapor pressure osmometer (Wescor, Logan, UT, USA) and Ψtlp (in MPa) was calculated as:$${Psi }_{tlp}=0.83{2Psi }_{osm}-0.631$$
    (4)
    Morphometric traitsThe morphometric trait data (Supplementary Table 2) were measured systematically by the same people (SPH and ICP) at all the sites. A standardized template for the field measurement of morphometric traits was used (Supplementary Table 5). This template provides a checklist of the traits and the categories used to describe them. The leaf traits assessed were texture, colour, size, thickness, orientation, display, shape, margin form, the presence of hairs, pubescence, pruinosity or rugosity, the presence of surface wax, hypostomatism, marginal curling (involute, revolute), smell (aromatic or fetid), the presence of a terminal notch or drip-tip, surface patterning, succulence, the presence and positioning of spines or thorns on the leaves. Illustrations of the various categories used in the classification of leaf margin and leaf shape are provided in supplementary materials, together with the template for leaf size categories (Supplementary Figs. 1–3). Although the distinction between spines and thorns is sometimes based on the source material (where thorns are derived from shoots and buds, and spines from any part of the leaf containing vascular material), here the differentiation is based on the shape of the protrusion (where thorns are triangular in shape and can be branched, and spines are unbranched and linear features). The checklist template also includes a limited amount of information on stem traits, such as form, colour, whether the stem is photosynthetic, the presence of stem hairs, pubescence, or pruinosity, and the presence of spines or thorns. For woody plants (trees, shrubs, climbers), the checklist also includes information on bark type (deciduous or not, with an indication of whether the bark is strip or chunk deciduous), the presence of furrowing, and also the presence of spines or thorns.Plant Functional TypesThe database includes information on life form, plant phenology, leaf form and leaf phenology (Table 8). Although these four pieces of information are used by many modellers in the definition of plant functional types (PFTs)69,70, they are not strictly species-specific traits. Thus, some species can occur as a tree, a small tree or a shrub (e.g. Cyclobalanopsis obovatifolia), or as a shrub or liana (e.g. Smilax discotis), depending on environmental conditions. Similarly, some species can behave as an evergreen or deciduous plant, depending on moisture availability (e.g. Ulmus parvifolia). Thus, this information is recorded for individual species at each site and no attempt was made to ensure that a given species was classified identically at all sites. In total 20 distinct life forms were recognized, including tree, small tree, low to high shrub, erect dwarf shrub, prostrate dwarf shrub, trailing shrub, liana, climber, forb, cushion forb, rosette forb, graminoid, bamboo, cycad, geophyte, stem succulent, succulent, pteridophyte, epiphyte, parasite. Plant phenology is recorded as perennial, biennial or annual. The primary distinction in leaf phenology is between deciduous and evergreen, but the classification used in the database also recognizes facultative deciduousness (semi-deciduous) and leaf-exchangers (i.e. plants that retain their leaves for nearly the whole year but drop and replace all of the leaves in a single short period, rather than replacing some leaves continuously through the year as evergreens do). The concept of leaf phenology is only relevant for woody plants (trees, shrubs, lianas) and so is not recorded for e.g. forbs or climbers.VegetationThe local vegetation was not recorded in the field at each site, and in any case such descriptions are hard to standardize. The CPTDv2 database contains information on vegetation type extracted from the digital vegetation map of China at the scale of 1:1 million71, which uses 55 plant communities (48 natural plant communities and seven cropping systems). CPTDv2 further provides information on vegetation clusters aggregated from those fundamental plant communities from the Vegetation Atlas of China based on their bioclimatic context72. CPTDv2 also contains information on potential natural vegetation (PNV), derived from an updated version of the73 global mapping of PNV. This PNV map was produced using pollen-based vegetation reconstructions as a target, a set of 160 spatially explicit co-variate data sets representing the climatic, topographic, geologic, and hydrological controls on plant growth and survival, and an ensemble machine-learning approach to account for the relationships between vegetation types and these covariates (Table 9). The original version of the map had a spatial resolution of 1 km; the updated version used here (https://github.com/Envirometrix/PNVmaps) has a resolution of 250 m.ClimateClimatological estimates of monthly temperature, precipitation and fraction of sunshine hours were derived from records from 1814 meteorological stations (740 stations have observations from 1971 to 2000, the rest from 1981 to 1990: China Meteorological Administration, unpublished data), interpolated to a 0.01 grid using a three-dimensional thin-plate spline (ANUSPLIN version 4.36;74. These monthly climatological data were used directly to calculate the mean temperature of the coldest month (MTCO), mean annual temperature (MAT), mean monthly precipitation (MMP) and mean annual precipitation (MAP). Bioclimatic variables at each site were calculated from the interpolated monthly temperature, precipitation and fraction of sunshine hours using the Simple Process-Led Algorithms for Simulating Habitats (SPLASH) model75. The bioclimatic variables include total annual photosynthetically active radiation during the growing season when mean daily temperatures are >0 °C (PAR0), the daily mean photosynthetically active radiation during the growing season (mPAR0), growing degree days above a baseline of 0 °C (GDD0), the daily mean temperature during the growing season (mGDD0), the ratio of actual to equilibrium evapotranspiration (α), and a moisture index (MI) defined as the ratio of mean annual precipitation to potential evapotranspiration. We also calculated the timing of peak rainfall and rainfall seasonality, using metrics described in Kelley, et al.76 (Supplementary Table 3).The topography in the Gongga region is complex, and the standard climate data set is inadequate to capture the elevation impacts of local climate at the sites there13. We therefore also provide alternative estimates of climatic variables for the Gongga elevation transects using 17 weather stations from the region with records from January 2017 to December 2019 (Supplementary Table 4). These 17 stations range in elevation from 422 m to 3951 m, in latitude from 28° to 31° N, and in longitude from 99.1° to 103.8° E. The climatological records for each station were downloaded from China Meteorological Data Service Centre, National Meteorological Information Centre (http://data.cma.cn/data/detail/dataCode/A.0012.0001.html). The monthly maximum and minimum temperature, precipitation, percentage of possible sunshine hours were extracted. The monthly mean temperature was calculated as the average of maximum and minimum temperature. The elevationally-sensitive ANUSPLIN interpolation scheme74 was used to provide estimates of meteorological variables at each site as described above. The bioclimatic variables were calculated following the same methodology as the 0.01 grid data described above.SoilSoil was not sampled in the field, but to facilitate analyses we provide soil information extracted from the Harmonized World Soil Database (HWSD) v1.277 (Table 10). The HWSD v1.2 is a high-resolution (0.05°) soil database with soil characteristics determined from real soil profiles. The soil properties were estimated in a harmonized way, where the actual soil profile data and the development of pedotransfer rules were undertaken in cooperation with ISRIC and ESBN drawing on the WISE soil profile database and some earlier works78,79. The HWSD v1.2 provides information for the uppermost soil layer (0–30 cm) and the deeper soil layer (30–100 cm). Although HWSD v1.2 contains information on a large number of soil properties, we only extracted information on soil texture (sand fraction, silt fraction and clay fraction), the content of organic carbon, soil pH in water, and cation exchange capacity. More

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    Infection with an acanthocephalan helminth reduces anxiety-like behaviour in crustacean host

    Cézilly, F. & Perrot-Minnot, M. J. Interpreting multidimensionality in parasite-induced phenotypic alterations: Panselectionism versus parsimony. Oikos 119, 1224–1229 (2010).Article 

    Google Scholar 
    Moore, J. Parasites and the Behavior of Animals. (Oxford University Press on Demand, 2002).
    Google Scholar 
    Thomas, F. et al. Do hairworms (Nematomorpha) manipulate the water seeking behaviour of their terrestrial hosts?. J. Evol. Biol. 15, 356–361 (2002).Article 

    Google Scholar 
    Weinersmith, K. L. What’s gotten into you? A review of recent research on parasitoid manipulation of host behavior. Curr. Opin. Insect Sci. 33, 37–42 (2019).Article 

    Google Scholar 
    Hughes, D. P. et al. Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection. BMC. Ecol. 11, (2011).Lagrue, C., Kaldonski, N., Perrot-Minnot, M. J., Motreuil, S. & Bollache, L. Modification of hosts’ behavior by a parasite: Field evidence for adaptive manipulation. Ecology 88, 2839–2847 (2007).Article 

    Google Scholar 
    Berdoy, M., Webster, J. P. & Mcdonald, D. W. Fatal attraction in rats infected with Toxoplasma gondii. Proc. R. Soc. B Biol. Sci. 267, 1591–1594 (2000).Article 
    CAS 

    Google Scholar 
    Perrot-Minnot, M. J., Kaldonski, N. & Cézilly, F. Increased susceptibility to predation and altered anti-predator behaviour in an acanthocephalan-infected amphipod. Int. J. Parasitol. 37, 645–651 (2007).Article 

    Google Scholar 
    Cézilly, F. & Perrot-Minnot, M. J. Studying adaptive changes in the behaviour of infected hosts: A long and winding road. Behav. Proc. 68, 223–228 (2005).Article 

    Google Scholar 
    Seppälä, O. & Jokela, J. Host manipulation as a parasite transmission strategy when manipulation is exploited by non-host predators. Biol. Lett. 4, 663–666 (2008).Article 

    Google Scholar 
    Dianne, L. et al. Protection first then facilitation: A manipulative parasite modulates the vulnerability to predation of its intermediate host according to its own developmental stage. Evolution 65, 2692–2698 (2011).Article 

    Google Scholar 
    Iritani, R. & Sato, T. Host-manipulation by trophically transmitted parasites: The switcher-paradigm. Trends Parasitol. 34, 934–944 (2018).Article 

    Google Scholar 
    Poulin, R. & Maure, F. Host manipulation by parasites: A look back before moving forward. Trends Parasitol. 31, 563–570 (2015).Article 

    Google Scholar 
    Herbison, R., Lagrue, C. & Poulin, R. The missing link in parasite manipulation of host behaviour. Parasite Vectors 11, 1–6 (2018).Article 

    Google Scholar 
    Perrot-Minnot, M. J. & Cézilly, F. Investigating candidate neuromodulatory systems underlying parasitic manipulation: Concepts, limitations and prospects. J. Exp. Biol. 216, 134–141 (2013).Article 

    Google Scholar 
    Adamo, S. A. Parasites: Evolution’s neurobiologists. J. Exp. Biol. 216, 3–10 (2013).Article 
    CAS 

    Google Scholar 
    Kaushik, M., Lamberton, P. H. L. & Webster, J. P. The role of parasites and pathogens in influencing generalised anxiety and predation-related fear in the mammalian central nervous system. Horm. Behav. 62, 191–201 (2012).Article 

    Google Scholar 
    Grupe, D. W. & Nitschke, J. B. Uncertainty and anticipation in anxiety: An integrated neurobiological and psychological perspective. Nat. Rev. Neurosci. 14, 488–501 (2013).Article 
    CAS 

    Google Scholar 
    Perry, C. J. & Baciadonna, L. Studying emotion in invertebrates: What has been done, what can be measured and what they can provide. J. Exp. Biol. 220, 3856–3868 (2017).Article 

    Google Scholar 
    Adamec, R. E., Burton, P., Shallow, T. & Budgell, J. NMDA receptors mediate lasting increases in anxiety-like behavior produced by the stress of predator exposure—Implications for anxiety associated with posttraumatic stress disorder. Physiol. Behav. 65, 723–737 (1998).Article 

    Google Scholar 
    Bacqué-Cazenave, J. et al. Serotonin in animal cognition and behavior. Int. J. Mol. Sci. 21, 1–23 (2020).Article 

    Google Scholar 
    Hamilton, T. J., Kwan, G. T., Gallup, J. & Tresguerres, M. Acute fluoxetine exposure alters crab anxiety-like behaviour, but not aggressiveness. Sci. Rep. 6, 4–9 (2016).Article 

    Google Scholar 
    de Bekker, C. et al. Gene expression during zombie ant biting behavior reflects the complexity underlying fungal parasitic behavioral manipulation. BMC Genom. 16, 1–23 (2015).Article 

    Google Scholar 
    Shaw, J. C. et al. Parasite manipulation of brain monoamines in California killifish (Fundulus parvipinnis) by the trematode Euhaplorchis californiensis. Proc. R. Soc. B Biol. Sci. 276, 1137–1146 (2009).Article 
    CAS 

    Google Scholar 
    Fayard, M., Dechaume-Moncharmont, F. X., Wattier, R. & Perrot-Minnot, M. J. Magnitude and direction of parasite-induced phenotypic alterations: A meta-analysis in acanthocephalans. Biol. Rev. 95, 1233–1251 (2020).Article 

    Google Scholar 
    Tain, L., Perrot-Minnot, M. J. & Cézilly, F. Altered host behaviour and brain serotonergic activity caused by acanthocephalans: Evidence for specificity. Proc. R. Soc. B Biol. Sci. 273, 3039–3045 (2006).Article 
    CAS 

    Google Scholar 
    Perrot-Minnot, M. J., Maddaleno, M., Balourdet, A. & Cézilly, F. Host manipulation revisited: No evidence for a causal link between altered photophobia and increased trophic transmission of amphipods infected with acanthocephalans. Funct. Ecol. 26, 1007–1014 (2012).Article 

    Google Scholar 
    Perrot-Minnot, M. J., Sanchez-Thirion, K. & Cézilly, F. Multidimensionality in host manipulation mimicked by serotonin injection. Proc. R. Soc. B Biol. Sci. 281, (2014).Perrot-Minnot, M. J., Banchetry, L. & Cézilly, F. Anxiety-like behaviour increases safety from fish predation in an amphipod crustacea. R. Soc. Open Sci. 4, (2017).Perrot-Minnot, M. J., Balourdet, A. & Musset, O. Optimization of anesthetic procedure in crustaceans: Evidence for sedative and analgesic-like effect of MS-222 using a semi-automated device for exposure to noxious stimulus. Aquat. Toxicol. 240, 105981 (2021).Article 
    CAS 

    Google Scholar 
    Barr, S., Laming, P. R., Dick, J. T. A. & Elwood, R. W. Nociception or pain in a decapod crustacean?. Anim. Behav. 75, 745–751 (2008).Article 

    Google Scholar 
    Fossat, P., Bacqué-Cazenave, J., de Deurwaerdère, P., Delbecque, J. P. & Cattaert, D. Anxiety-like behavior in crayfish is controlled by serotonin. Science 1979(344), 1293–1297 (2014).Article 
    ADS 

    Google Scholar 
    Magee, B. & Elwood, R. W. Shock avoidance by discrimination learning in the shore crab (Carcinus maenas) is consistent with a key criterion for pain. J. Exp. Biol. 216, 353–358 (2013).Article 

    Google Scholar 
    Rakitin, A., Tomsic, D. & Maldonado, H. Habituation and sensitization to an electrical shock in the crab Chasmagnathus. Effect of background illumination. Physiol. Behav. 50, 477–487 (1991).Article 
    CAS 

    Google Scholar 
    Koolhaas, J. M. et al. Stress revisited: A critical evaluation of the stress concept. Neurosci. Biobehav. Rev. 35, 1291–1301 (2011).Article 
    CAS 

    Google Scholar 
    Yuan, T. F. & Hou, G. The effects of stress on glutamatergic transmission in the brain. Mol. Neurobiol. 51, 1139–1143 (2015).Article 
    CAS 

    Google Scholar 
    Fossat, P., Bacqué-Cazenave, J., de Deurwaerdère, P., Cattaert, D. & Delbecque, J. P. Serotonin, but not dopamine, controls the stress response and anxiety-like behavior in the crayfish Procambarus clarkii. J. Exp. Biol. 218, 2745–2752 (2015).
    Google Scholar 
    Benesh, D. P., Valtonen, E. T. & Seppälä, O. Multidimensionality and intra-individual variation in host manipulation by an acanthocephalan. Parasitology 135, 617–626 (2008).Article 
    CAS 

    Google Scholar 
    Kaldonski, N., Perrot-Minnot, M. J. & Cézilly, F. Differential influence of two acanthocephalan parasites on the antipredator behaviour of their common intermediate host. Anim. Behav. 74, 1311–1317 (2007).Article 

    Google Scholar 
    Kaldonski, N., Perrot-Minnot, M. J., Motreuil, S. & Cézilly, F. Infection with acanthocephalans increases the vulnerability of Gammarus pulex (Crustacea, Amphipoda) to non-host invertebrate predators. Parasitology 135, 627–632 (2008).Article 
    CAS 

    Google Scholar 
    Parker, G. A., Ball, M. A., Chubb, J. C., Hammerschmidt, K. & Milinski, M. When should a trophically transmitted parasite manipulate its host?. Evolution 63, 448–458 (2009).Article 

    Google Scholar 
    Paul, E. S. & Mendl, M. T. Animal emotion: Descriptive and prescriptive definitions and their implications for a comparative perspective. Appl. Anim. Behav. Sci. 205, 202–209 (2018).Article 

    Google Scholar 
    Anderson, D. J. & Adolphs, R. A framework for studying emotions across species. Cell 157, 187–200 (2014).Article 
    CAS 

    Google Scholar 
    Weinberger, J. & Klaper, R. Environmental concentrations of the selective serotonin reuptake inhibitor fluoxetine impact specific behaviors involved in reproduction, feeding and predator avoidance in the fish Pimephales promelas (fathead minnow). Aquat. Toxicol. 151, 77–83 (2014).Article 
    CAS 

    Google Scholar 
    Curran, K. P. & Chalasani, S. H. Serotonin circuits and anxiety: What can invertebrates teach us?. Invertebr. Neurosci. 12, 81–92 (2012).CAS 

    Google Scholar 
    Mohammad, F. et al. Ancient anxiety pathways influence Drosophila defense behaviors. Curr. Biol. 26, 981–986 (2016).Article 
    CAS 

    Google Scholar 
    Kavaliers, M. & Colwell, D. D. Decreased predator avoidance in parasitized mice: neuromodulatory correlates. Parasitology 111, 257–263 (1995).Article 

    Google Scholar 
    Chivers, D. P., Wisenden, B. D. & Smith, R. J. F. Damselfly larvae learn to recognize predators from chemical cues in the predator’s diet. Anim. Behav. 52, 315–320 (1996).Article 

    Google Scholar 
    Hazlett, B. A., Acquistapace, P. & Gherardi, F. Differences in memory capabilities in invasive and native crayfish. J. Crustac. Biol. 22, 439–448 (2002).Article 

    Google Scholar 
    R Core Team. R Core Team (2014). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. R Foundation for Statistical Computing (2014). More

  • in

    Seasonal variation in daily activity patterns of snow leopards and their prey

    Lima, S. L. & Dill, L. M. Behavioral decisions made under the risk of predation: A review and prospectus. Can. J. Zool. 68, 619–640 (1990).Article 

    Google Scholar 
    Ordiz, A., Stoen, O. G., Delibes, M. & Swenson, J. E. Predators or prey? Spatio-temporal discrimination of human-derived risk by brown bears. Oecologia 166, 59–67 (2011).Article 
    ADS 

    Google Scholar 
    Glass, T. W., Breed, G. A., Robards, M. D., Williams, C. T. & Kielland, K. Trade-off between predation risk and behavioural thermoregulation drives resting behaviour in a cold-adapted mesocarnivore. Anim. Behav. 175, 163–174 (2021).Article 

    Google Scholar 
    Daan, S. & Aschoff, J. Circadian rhytms of locomotor activity in captive birds and mammals: Their variation with seasons and latitude. Oecologia 18, 269–316 (1975).Article 
    ADS 

    Google Scholar 
    Kronfeld-Schor, N. & Dayan, T. Partitioning of time as an ecological resource. Annu. Rev. Ecol. Evol. Syst. 34, 153–181 (2003).Article 

    Google Scholar 
    Garcia, R. A., Cabeza, M., Rahbek, C. & Araujo, M. B. Multiple dimensions of climate change and their implications for biodiversity. Science 344, 1247579 (2014).Article 

    Google Scholar 
    Curio, E. The Ethology of Predation (Springer-Verlag, 1976).Book 

    Google Scholar 
    Linkie, M. & Ridout, M. S. Assessing tiger-prey interactions in Sumatran rainforests. J. Zool. 284, 224–229 (2011).Article 

    Google Scholar 
    Heurich, M. et al. Activity patterns of Eurasian lynx are modulated by light regime and individual traits over a wide latitudinal range. PLoS ONE 9, e114143 (2014).Article 
    ADS 

    Google Scholar 
    Harmsen, B. J., Foster, R. J., Silver, S. C., Ostro, L. E. T. & Doncaster, C. P. Jaguar and puma activity patterns in relation to their main prey. Mamm. Biol. 76, 320–324 (2011).Article 

    Google Scholar 
    Foster, V. C. et al. Jaguar and puma activity patterns and predator-prey interactions in four Brazilian biomes. Biotropica 45, 373–379 (2013).Article 

    Google Scholar 
    Theuerkauf, J. et al. Daily patterns and duration of wolf activity in the Bialowieza forest, Poland. J. Mammal. 84, 243–253 (2003).Article 

    Google Scholar 
    Hebblewhite, M., Merrill, E. H. & McDonald, T. L. Spatial decomposition of predation risk usign resource selection functions: An example in a wolf-elk predator-prey system. Oikos 111, 101–111 (2005).Article 

    Google Scholar 
    Balme, G., Hunter, L. & Slotow, R. Feeding habitat selection by hunting leopards Panthera pardus in a woodland Savanna: Prey catchability versus abundance. Anim. Behav. 74, 589–598 (2007).Article 

    Google Scholar 
    Smith, J. A. et al. Where and when to hunt? Decomposing predation success of an ambush carnivore. Ecology 101, e03172 (2020).Article 

    Google Scholar 
    Hopcraft, J. G. C., Sinclair, A. R. E. & Packer, C. Planning for success: Serengeti lions seek prey accessibility rather than abundance. J. Anim. Ecol. 74, 559–566 (2005).Article 

    Google Scholar 
    Theuerkauf, J. What drives wolves: Fear or hunger? Humans, diet, climate and wolf activity patterns. Ethology 115, 649–657 (2009).Article 

    Google Scholar 
    Funston, P. J., Mills, M. G. & Biggs, H. C. Factors affecting the hunting success of male and female lions in the Kruger National Park. J. Zool. 253, 419–431 (2001).Article 

    Google Scholar 
    Schaller, G. The Serengeti lion (The University of Chicago Press, IL, 1972).
    Google Scholar 
    Bailey, T. N. The African Leopard, Ecology and Behaviour of a Solitary Felid (The Blackburn Press, 1993).Book 

    Google Scholar 
    Jenny, D. & Zuberbühler, K. Hunting behaviour in West African forest leopards. Afr. J. Ecol. 43, 197–200 (2005).Article 

    Google Scholar 
    Packer, C., Swanson, A., Ikanda, D. & Kushnir, H. Fear of darkness, the full moon and the nocturnal ecology of African lions. PLoS ONE 6, e22285 (2011).Article 
    ADS 
    CAS 

    Google Scholar 
    Palmer, M. S., Fieberg, J., Swanson, A., Kosmala, M. & Packer, C. A “dynamic” landscape of fear: Prey responses to spatiotemporal variations in predation risk across the lunar cycle. Ecol. Letters 20, 1364–1373 (2017).Article 
    CAS 

    Google Scholar 
    Steinmetz, R., Seuaturien, N. & Chutipong, W. Tigers, leopards, and dholes in a half-empty forest: Assessing species interactions in a guild of threatened carnivores. Biol. Cons. 163, 68–78 (2013).Article 

    Google Scholar 
    Carter, N., Jasny, M., Gurung, B. & Liu, J. Impacts of people and tigers on leopard spatiotemporal activity patterns in a global biodiversity hotspot. Global Ecol. Conserv. 3, 149–162 (2015).Article 

    Google Scholar 
    George, S. L. & Crooks, K. R. Recreation and large mammal activity in an urban nature reserve. Biol. Cons. 133, 107–117 (2006).Article 

    Google Scholar 
    Beltrán, J. F. & Delibes, M. Environmental determinants of circadian activity of free-ranging Iberian lynxes. J. Mammal. 75, 382–393 (1994).Article 

    Google Scholar 
    McNab, B. K. The standard energetics of mammalian carnivores: Felidae and Hyaenidae. Sikes Can. J. Zool. 78, 2227–2239 (2000).Article 

    Google Scholar 
    Mishra, C. et al. Increasing risks for emerging infectious diseases within a rapidly changing High Asia. Ambio 51, 494–507 (2022).Article 

    Google Scholar 
    Mishra, C., Redpath, S. M. & Suryawanshi, K. R. Livestock predation by snow leopards: Conflicts and the search for solutions. In Snow Leopards (eds McCarthy, T. M. & Mallon, D.) 59–67 (Academic Press, 2016).Chapter 

    Google Scholar 
    Farrington, J. D., and J. Li. 2016. Climate change impacts on snow leopard range. In: McCarthy, T.M., Mallon, D., editors. Snow Leopards. Academic Press.Jackson, R. Home Range, Movements and Habitat use of Snow Leopard in Nepal (Dissertation niversity of London, London, 1996).
    Google Scholar 
    McCarthy, T. M., Fuller, T. K. & Munkhtsog, B. Movements and activities of snow leopards in Southwestern Mongolia. Biol. Cons. 124, 527–537 (2005).Article 

    Google Scholar 
    Salvatori, M. et al. Co-occurrence of snow leopard, wolf and Siberian ibex under livestock encroachment into protected areas across the Mongolian Altai. Biol. Cons. 261, 109294 (2021).Article 

    Google Scholar 
    Rode, J. et al. Population monitoring of snow leopards using camera trapping in Naryn state nature reserve, Kyrgyzstan, between 2016 and 2019. Global Ecol. Conserv. 31, e01850 (2021).Article 

    Google Scholar 
    Sharma, R. K. et al. Spatial variation in population-density of snow leopards in a multiple use landscape in Spiti Valley Trans-Himalay. PLoS ONE 16, e0250900 (2021).Article 
    CAS 

    Google Scholar 
    Kachel, S. M., Karimov, K. & Wirsing, A. J. Predator niche overlap and partitioning and potential interactions in the mountains of Central Asia. J. Mammal. 103, 1019–1029 (2022).Article 

    Google Scholar 
    Johansson, Ö., Simms, A. & McCarthy, T. M. From VHF to satellite GPS collars: Advancements in snow leopard telemetry. In Snow leopards (eds McCarthy, T. M. & Mallon, D.) p355-365 (Academic Press, 2016).Chapter 

    Google Scholar 
    Johansson, Ö. et al. Snow leopard predation in a livestock dominated landscape in Mongolia. Biol. Cons. 184, 251–258 (2015).Article 

    Google Scholar 
    Havmøller, R. W., Jacobsen, N. S., Scharff, N., Rovero, F. & Zimmermann, F. Assessing the activity pattern overlap among leopards (Panthera pardus), potential prey and competitors in a complex landscape in Tanzania. J. Zool. 311, 175–182 (2020).Article 

    Google Scholar 
    Kitchener, A. C., Van Valkenburgh, B. & Yamaguchi, N. Felid form and function. In Biology and Conservation of Wild Felids (eds MacDonald, D. W. & Loveridge, A. J.) 83–106 (Oxford University Press, 2010).
    Google Scholar 
    Fuglesteg, B. N., Haga, Ø. E., Folkow, L. P., Fuglei, E. & Blix, A. S. Seasonal variations in basal metabolic rate, lower critical temperature and responses to temporary starvation in the arctic fox (Alopex lagopus) from Svalbard. Polar Biol. 29, 308–319 (2005).Article 

    Google Scholar 
    Doris, P. A. & Baker, M. A. Effect of dehydration on thermoregulation in cats exposed to high ambient temperatures. J. Appl. Physiol. 51, 46–54 (1981).Article 
    CAS 

    Google Scholar 
    Forrest, J. L. et al. Conservation and climate change: Assessing the vulnerability of snow leopard habitat to treeline shift in the Himalaya. Biol. Cons. 150, 129–135 (2012).Article 

    Google Scholar 
    Sharma, R. K., Bhatnagar, Y. V. & Mishra, C. Does livestock benefit or harm snow leopards?. Biol. Cons. 190, 8–13 (2015).Article 

    Google Scholar 
    Samelius, G. et al. Keeping predators out: Testing fences to reduce livestock depredation at night-time corrals. Oryx 55, 466–472 (2021).Article 

    Google Scholar 
    Hebblewhite, M. & Merrill, E. Modelling wildlife-human relationships for social species with mixed-effects resource selection models. J. Appl. Ecol. 45, 834–844 (2007).Article 

    Google Scholar 
    Johansson, Ö., Malmsten, J., Mishra, C., Lkhagvajav, P. & McCarthy, T. Reversible immobilization of free-ranging snow leopards (Panthera uncia) with a combination of medetomidine and tiletamine-zolazepam. J. Wildl. Dis. 49, 338–346 (2013).Article 

    Google Scholar 
    Johansson, Ö., Kachel, S. & Weckworth, B. Guidelines for telemetry studies on snow leopards. Animals 12, 1663 (2022).Article 

    Google Scholar 
    Bjørneraas, K., Van Moorter, B., Rolandsen, C. M. & Herfindal, I. Screening global positioning system location data for errors using animal movement characteristics. J. Wildl. Manag. 74, 1361–1366 (2010).Article 

    Google Scholar 
    Pålsson O. 2022. Maternal behaviour of the snow leopard (Panthera uncial). MSc thesis. Uppsala University, Uppsala; Sweden https://www.diva-portal.org/smash/get/diva2:1668965/FULLTEXT01.pdf.du Sert, N. P. et al. Reporting animal research: Explanation and elaboration for the ARRIVE guidelines 20. PLoS Biol. 18, e3000411 (2020).Article 

    Google Scholar 
    Nygren, E. 2015. Activity patterns of snow leopards (Panthera uncia) at their kill sites. MSc thesis, Swedish University of Agricultural Sciences, Uppsala, Sweden. https://stud.epsilon.slu.se/8109/1/nygren_e_150625.pdf.Johansson, Ö. et al. Land sharing is essential for snow leopard conservation. Biol. Cons. 203, 1–7 (2016).Article 

    Google Scholar 
    Johansson, Ö. et al. The timing of breeding and independence for snow leopard females and their cubs. Mamm. Biol. 101, 173–180 (2021).Article 

    Google Scholar 
    Nouvellet, P., Rasmussen, G. S. A., Macdonald, D. W., Courchamp, F. & Braae, A. Noisy clocks and silent sunrises: Measurement methods of daily activity pattern. J. Zool. 286, 179–184 (2012).Article 

    Google Scholar 
    Ridout, M. S. & Linkie, M. Estimating overlap of daily activity patterns from camera trap data. J. Agric. Biol. Environ. Stat. 14, 322–337 (2009).Article 
    MathSciNet 
    MATH 

    Google Scholar 
    R Development core team. 2019. R: A language and environment for statistical computing. R foundation for statistical computing Vienna, Austria. www.R-project.org/.Wood, S. N. Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J. Roy. Stat. Soc. B 73, 3–36 (2011).Article 
    MathSciNet 
    MATH 

    Google Scholar  More

  • in

    Nature’s biggest news stories of 2022

    Russia invades UkraineThe global science community was quick to condemn Russian’s invasion of Ukraine in February. Research organizations moved fast to cut ties with Russia, stopping funding and collaborations, and journals came under pressure to boycott Russian authors.The situation escalated when Russian forces attacked Europe’s largest nuclear power plant, Zaporizhzhia, in March, prompting fears of a nuclear accident. Russian troops continue to occupy the power plant. Since the invasion began, thousands of civilians have been killed and millions displaced; many others, including scientists, have fled the country.The war has affected research in space and climate science, disrupted fieldwork and played a significant part in the global energy crisis. The invasion could also precipitate a new era for European defence research.JWST delights astronomers

    Stephans Quintet, a grouping of five galaxies, taken by NASA’s James Webb Space Telescope.Credit: NASA, ESA, CSA, and STScI via Getty

    NASA’s James Webb Space Telescope (JWST) — the most complex telescope ever built — reached its destination in space in January after decades of planning. In July, astronomers were awed by the telescope’s first image — of thousands of distant galaxies in the constellation Volans. Since then, the US$10-billion observatory has captured a steady stream of spectacular images, and astronomers have been working feverishly on early data. Insights include detailed observations of an exoplanet, and leading contenders for the most distant galaxy ever seen.NASA also decided not to rename the telescope, despite calls from some astronomers to do so because the telescope’s namesake, a former NASA administrator, held high-ranking government positions in the 1950s and 1960s, when the United States systematically fired gay and lesbian government employees. A NASA investigation “found no evidence that Webb was either a leader or proponent of firing government employees for their sexual orientation”, the agency said in a statement in November.AI predicts protein structuresResearchers announced in July that they had used the revolutionary artificial-intelligence (AI) network AlphaFold to predict the structures of more than 200 million proteins from roughly one million species, covering almost every known protein from all organisms whose genomes are held in databases. The development of AlphaFold netted its creators at the London-based AI company DeepMind, owned by Alphabet, one of this year’s US$3-million Breakthrough prizes — the most lucrative awards in science.AlphaFold isn’t the only player on the scene. Meta (formerly Facebook), in California, has developed its own AI network, called ESMFold, and used it to predict the shapes of roughly 600 million possible proteins from bacteria, viruses and other microorganisms that have not been isolated or cultured. Scientists are using these tools to dream up proteins that could form the basis of new drugs and vaccines.Monkeypox goes global

    The monkeypox virus (shown here as a coloured transmission electron micrograph) is related to the smallpox virus.Credit: CDC/Science Photo Library

    The rapid global spread of monkeypox (recently renamed ‘mpox’ by the World Health Organization) this year caught many scientists off guard. Previously, the virus had mainly been confined to Central and West Africa, but from May this year, infections started appearing in Europe, the United States, Canada and many other countries, mostly in young and middle-aged men who have sex with men. The virus is related to smallpox, and the circulating strain only rarely causes severe disease or death. But its fast spread led the World Health Organization to declare the global outbreak a ‘public-health emergency of international concern’, the agency’s highest alert level, in July.As cases soared, researchers got to work trying to understand the dynamics of the disease. Studies confirmed that it is transmitted primarily through repeated skin-to-skin contact, and trials of possible treatments got under way. Existing smallpox vaccines were also used to suppress the virus in some countries. Six months after mpox infections first started increasing, vaccination efforts and behavioural changes seemed to have curbed its spread in Europe and the United States. Researchers predict a range of scenarios from here — the most hopeful being that the virus fizzles out in non-endemic countries over the next few months or years.The Moon has a revivalThe Moon has become a popular destination for space missions this year. First off the launch pad, in August, was South Korea’s Danuri probe, which is expected to arrive at its destination in January and orbit the Moon for a year. The mission is the country’s first foray beyond Earth’s orbit and is carrying a host of experiments.Last month, NASA’s hotly anticipated Artemis programme — which aims to send astronauts to the Moon in the next few years — finally kicked off with the launch of an uncrewed capsule called Orion, a joint venture with the European Space Agency. As part of a test flight to see whether the system can transport people safely to the Moon, the capsule flew out past the Moon and made its way back to Earth safely this month.A lunar spacecraft made by a Japanese company launched this month. ispace’s M1 lander is aiming to be the first of several private ventures to land on the surface of the Moon next year. The lander will carry two rovers, one for the United Arab Emirates and another for the Japan Aerospace Exploration Agency, JAXA. The rovers will be a first for both countries.Climate-change funding

    People cross a flooded highway in Sindh province, Pakistan in August.Credit: Waqar Hussein/EPA-EFE/Shutterstock

    There were many reasons to feel despondent about the United Nations Climate Change Conference of the Parties (COP27) in Egypt last month, but an agreement on a new ‘loss and damage’ fund was one bright spot. The fund will help low- and middle-income countries to cover the cost of climate-change impacts, such as the catastrophic floods in Pakistan this year, which caused more than US$30 billion worth of damage and economic losses.But calls at COP27 to phase out fossil fuels were blocked by oil-producing states, and many blamed the lack of progress on the energy crisis sparked by Russia’s invasion of Ukraine. High natural-gas prices have led some European nations to rely temporarily on coal. Global carbon emissions from fossil fuels are expected to hit 37.5 billion tonnes this year, a new record. The window to limit warming to 1.5–2 ºC above pre-industrial temperatures is disappearing fast — and might even have passed.Omicron’s offspring drive the pandemicOmicron and its descendants dominated all other coronavirus variants this year. The fast-spreading strain was first detected in southern Africa in November 2021, and quickly spread around the globe. From early on, it was clear that Omicron could evade immune-system defences more successfully than previous variants, which has meant that vaccines are less effective. Throughout the year, a diverse group of immune-dodging offshoots of Omicron has emerged, making it challenging for scientists to predict coming waves of infection.Vaccines based on Omicron variants have been rolled out in some countries in the hope they will offer greater protection than previous jabs, but early data suggest the extra benefit is modest. Nasal sprays against COVID-19 have also become a tool in the vaccine arsenal. The idea is that these stop the virus at the site where it first takes hold. In September, China and India approved needle-free COVID-19 vaccines that are delivered through the nose or mouth, and many similar vaccines are in various stages of development.Pig organs transplanted into people

    Surgeons in Baltimore, Maryland transplanted the first pig heart into a person in January.Credit: EyePress News/Shutterstock

    In January, US handyman David Bennett became the first person to receive a transplanted heart from a genetically modified pig — a crucial first step in determining whether animals could provide a source of organs for people who need them. Bennett survived for another eight weeks after the transplant, but researchers were impressed that he lived for that long, given that the human immune system attacks non-genetically modified pig organs in minutes. A few months later, two US research groups independently reported transplanting pig kidneys into three people who had been declared legally dead because they did not have brain function. The organs weren’t rejected and started producing urine. Researchers say the next step is clinical trials to test such procedures thoroughly in living people.Elections and science

    Luís Inácio Lula da Silva was elected president of Brazil in October.Credit: Fabio Vieira/FotoRua/NurPhoto via Getty

    National elections in Brazil, Australia and France brought relief for many researchers. After three years of science-damaging policies under right-wing president Jair Bolsonaro, Brazil narrowly elected leftist labour leader and former president Luiz Inácio Lula da Silva to lead the country in October. Scientists are hopeful that Lula’s return will result in a desperately needed boost to research funding and greater protection for the Amazon rainforest.French researchers were buoyed by President Emmanuel Macron’s victory over far-right candidate Marine Le Pen in April, and the election of Anthony Albanese as prime minister in Australia in May was seen as a good thing for science and climate-change action, too. In China, Xi Jinping cemented his legacy with an historic third term as head of the Chinese Communist Party. Xi has placed science and innovation at the heart of his country’s growth strategy.In other nations, it was unclear how research would fare under new leaders, such as Giorgia Meloni, the far-right candidate elected as Italy’s first female prime minister in October. Science was not a priority for the United Kingdom’s three prime ministers this year, although they have retained previous commitments to raise research funding. After Boris Johnson reisgned, Liz Truss was in the position for just seven weeks before she too resigned and the current Prime Minister Rishi Sunak took over.Environmental push beginsThis week, conservation and political leaders are attempting to finalize a global deal to protect the environment. The UN’s Convention on Biological Diversity Conference of the Parties (COP15) is under way in Montreal, Canada. A new biodiversity treaty, known as the post-2020 Global Diversity Framework, has been delayed by more than two years because of the COVID-19 pandemic. Progress towards an agreement has been slow, and the deal looked under threat when negotiations stalled over financing during international talks in Nairobi in June. Financial pledges from some nations to support biodiversity helped discussions to move forward, but estimates suggest that US$700 billion more is needed annually to protect the natural world. At the meeting, delegates will hopefully agree on targets to stabilize species’ declines by 2030 and reverse them by mid-century. More