More stories

  • in

    Song complexity is maintained during inter-population cultural transmission of humpback whale songs

    Rendell, L. & Whitehead, H. Culture in whales and dolphins. Behav. Brain Sci. 24, 309–324 (2001).CAS 
    Article 

    Google Scholar 
    Krützen, M. et al. Cultural transmission of tool use in bottlenose dolphins. Proc. Natl. Acad. Sci. U.S.A. 102, 8939–8943 (2005).ADS 
    Article 

    Google Scholar 
    Kawai, M. Newly-acquired pre-cultural behavior of the natural troop of Japanese monkeys on Koshima Islet. Primates 6, 1–30 (1965).Article 

    Google Scholar 
    Slater, P. The cultural transmission of bird song. Trends Ecol. Evol. 1, 94–97 (1986).CAS 
    Article 

    Google Scholar 
    Whitehead, H. & Rendell, L. The cultural lives of whales and dolphins. (University of Chicago Press, 2014).Whiten, A. The identification and differentiation of culture in chimpanzees and other animals: from natural history to diffusion experiments. The question of animal culture, 99–124 (2009).Allen, J. A. Community through culture: from insects to whales: How social learning and culture manifest across diverse animal communities. BioEssays 41, 1900060 (2019).Article 

    Google Scholar 
    Allen, J., Weinrich, M., Hoppitt, W. & Rendell, L. Network-based diffusion analysis reveals cultural transmission of lobtail feeding in humpback whales. Science 340, 485–488 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    Baker, C. Migratory movement and population structure of humpback whales (Megaptera novaeangliae) in the central and eastern North Pacific. Mar Ecol Prog Ser 31, 105–119 (1986).ADS 
    Article 

    Google Scholar 
    Garrigue, C. et al. Movement of individual humpback whales between wintering grounds of Oceania (South Pacific), 1999 to 2004. J. Cetacean Res. Manage 3, 275–281 (2011).
    Google Scholar 
    Rosenbaum, H. C. et al. First circumglobal assessment of Southern Hemisphere humpback whale mitochondrial genetic variation and implications for management. Endang. Spec. Res. 32, 551–567 (2017).Article 

    Google Scholar 
    Noad, M. J., Cato, D. H., Bryden, M. M., Jenner, M. N. & Jenner, K. C. Cultural revolution in whale songs. Nature 408, 537. https://doi.org/10.1038/35046199 (2000).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Payne, R. S. & McVay, S. Songs of humpback whales. Science 173, 585–597 (1971).ADS 
    CAS 
    Article 

    Google Scholar 
    Garland, E. C. et al. Dynamic horizontal cultural transmission of humpback whale song at the ocean basin scale. Curr. Biol. 21, 687–691. https://doi.org/10.1016/j.cub.2011.03.019 (2011).CAS 
    Article 
    PubMed 

    Google Scholar 
    Payne, R. & Guinee, L. N. Humpback whale (Megaptera novaeangliae) songs as an indicator of “stocks”. Communication and behavior of whales, 333–358 (1983).Garrigue, C. et al. Movements of humpback whales in Oceania, South Pacific. J. Cetac. Res. Manage. 4, 255–260 (2002).
    Google Scholar 
    Derville, S., Torres, L. G., Zerbini, A. N., Oremus, M. & Garrigue, C. Horizontal and vertical movements of humpback whales inform the use of critical pelagic habitats in the western South Pacific. Sci. Rep. 10, 1–13 (2020).Article 

    Google Scholar 
    Garrigue, C. et al. First assessment of interchange of humpback whales between Oceania and the East coast of Australia. J. Cetac. Res. Manage. 3, 269–274 (2011).
    Google Scholar 
    Steel, D. et al. Migratory connections between humpback whales from South Pacific breeding grounds and Antarctic feeding areas based on genotype matching. Int. Whal. Comm. (2008).Constantine, R., Russell, K., Gibbs, N., Childerhouse, S. & Baker, C. S. Photo-identification of humpback whales (Megaptera novaeangliae) in New Zealand waters and their migratory connections to breeding grounds of Oceania. Mar. Mam. Sci. 23, 715–720 (2007).Article 

    Google Scholar 
    Garland, E. C. et al. Humpback whale song on the southern ocean feeding grounds: implications for cultural transmission. PLoS ONE 8, e79422 (2013).ADS 
    Article 

    Google Scholar 
    Garland, E. C. et al. Population structure of humpback whales in the western and central South Pacific Ocean as determined by vocal exchange among populations. Conserv. Biol. 29, 1198–1207 (2015).Article 

    Google Scholar 
    Cholewiak, D. M., Sousa-Lima, R. S. & Cerchio, S. Humpback whale song hierarchical structure: Historical context and discussion of current classification issues. Mar. Mam. Sci. 29, E312–E332. https://doi.org/10.1111/mms.12005 (2013).Article 

    Google Scholar 
    Payne, K., Tyack, P. & Payne, R. Progressive changes in the songs of humpback whales (Megaptera novaeangliae): a detailed analysis of two seasons in Hawaii. Communication and behavior of whales, 9–57 (1983).Payne, K. & Payne, R. Large scale changes over 19 years in songs of humpback whales in Bermuda. Ethology 68, 89–114 (1985).
    Google Scholar 
    Allen, J. A., Garland, E. C., Dunlop, R. A. & Noad, M. J. Cultural revolutions reduce complexity in the songs of humpback whales. Proc. R. Soc. B: Biol. Sci. 285, 20182088. https://doi.org/10.1098/rspb.2018.2088 (2018).Article 

    Google Scholar 
    Allen, J. A., Garland, E. C., Murray, A., Noad, M. J. & Dunlop, R. Using self-organizing maps to classify humpback whale song units and quantify their similarity. J. Acoust. Soc. Am. 142, 1943–1952 (2017).ADS 
    Article 

    Google Scholar 
    Murray, A., Dunlop, R. A., Noad, M. J. & Goldizen, A. W. Stereotypic and complex phrase types provide structural evidence for a multi-message display in humpback whales (Megaptera novaeangliae). J Acoust Soc Am. 143, 980–994 (2018).ADS 
    Article 

    Google Scholar 
    Garland, E. C. et al. Redefining western and central South Pacific humpback whale population structure based on vocal cultural exchange. (2013).Rekdahl, M. Humpback whale vocal communication: Use and stability of social calls and revolutions in the songs of east Australian whales. (2012).Templeton, C. N., Laland, K. N. & Boogert, N. J. Does song complexity correlate with problem-solving performance in flocks of zebra finches?. Anim. Behav. 92, 63–71 (2014).Article 

    Google Scholar 
    Boogert, N. J., Giraldeau, L.-A. & Lefebvre, L. Song complexity correlates with learning ability in zebra finch males. Anim. Behav. 76, 1735–1741 (2008).Article 

    Google Scholar 
    Winn, H. & Winn, L. The song of the humpback whale Megaptera novaeangliae in the West Indies. Mar. Biol. 47, 97–114 (1978).Article 

    Google Scholar 
    Girola, E., Noad, M. J., Dunlop, R. A. & Cato, D. H. Source levels of humpback whales decrease with frequency suggesting an air-filled resonator is used in sound production. The Journal of the Acoustical Society of America (In Review).Warren, V. E., Constantine, R., Noad, M., Garrigue, C. & Garland, E. C. Migratory insights from singing humpback whales recorded around central New Zealand. R. Soc. Open Sci. 7, 201084 (2020).ADS 
    Article 

    Google Scholar 
    Garland, E. C. et al. Quantifying humpback whale song sequences to understand the dynamics of song exchange at the ocean basin scale. J. Acoust. Soc. Am. 133, 560–569. https://doi.org/10.1121/1.4770232 (2013).ADS 
    Article 
    PubMed 

    Google Scholar 
    Owen, C. et al. Migratory convergence facilitates cultural transmission of humpback whale song. R. Soc. Open Sci. 6, 190337 (2019).ADS 
    Article 

    Google Scholar 
    Garland, E. C., Rendell, L., Lamoni, L., Poole, M. M. & Noad, M. Song hybridization events during revolutionary song change provide insights into cultural transmission in humpback whales. Proc. Natl. Acad. Sci. 114, 7822–7829 (2017).CAS 
    Article 

    Google Scholar 
    Noad, M. & Cato, D. A combined acoustic and visual survey of humpback whales off southeast Queensland. Mem. Qld. Mus. 47, 507–523 (2001).
    Google Scholar 
    Spierings, M., de Weger, A. & Ten Cate, C. Pauses enhance chunk recognition in song element strings by zebra finches. Anim. Cogn. 18, 867–874 (2015).Article 

    Google Scholar 
    Doupe, A. J. & Kuhl, P. K. Birdsong and human speech: common themes and mechanisms. Annu. Rev. Neurosci. 22, 567–631 (1999).CAS 
    Article 

    Google Scholar 
    Allen, J. A., Garland, E. C., Dunlop, R. A. & Noad, M. J. Network analysis reveals underlying syntactic features in a vocally learnt mammalian display, humpback whale song. Proc. R. Soc. B 286, 20192014 (2019).Article 

    Google Scholar 
    Barón Birchenall, L. Animal communication and human language: An overview. International Journal of Comparative Psychology 29 (2016).Noad, M. J. The use of song by humpback whales (Megaptera novaeangliae) during migration off the east coast of Australia (doctoral dissertation) Doctor of Philosophy thesis, University of Sydney, (2002).Catchpole, C. Song and female choice: good genes and big brains?. Trends Ecol. Evol. 11, 358–360. https://doi.org/10.1016/0169-5347(96)30042-6 (1996).CAS 
    Article 
    PubMed 

    Google Scholar 
    Nowicki, S., Hasselquist, D., Bensch, S. & Peters, S. Nestling growth and song repertoire size in great reed warblers: evidence for song learning as an indicator mechanism in mate choice. Proc. R. Soc. London B: Biol. Sci. 267, 2419–2424 (2000).CAS 
    Article 

    Google Scholar 
    NOAA. Vol. 81 (ed National Marine Fisheries Service) 62260–62320 (Department of Commerce, Federal Register, 2016).Noad, M. J., Kniest, E. & Dunlop, R. A. Boom to bust? Implications for the continued rapid growth of the eastern Australian humpback whale population despite recovery. Popul. Ecol. 61(2), 198–209 (2019).Article 

    Google Scholar 
    Garrigue, C., Albertson, R. & Jackson, J. A. An anomalous increase in the New Caledonia humpback whales breeding sub-stock E2. Scientific Committee of the International Whaling Commission, Paper (2012).Garland, E. C. & McGregor, P. K. Cultural transmission, evolution, and revolution in vocal displays: Insights from bird and whale song. Front. Psychol. 11, 2387 (2020).Article 

    Google Scholar 
    Zandberg, L., Lachlan, R. F., Lamoni, L. & Garland, E. C. Global cultural evolutionary model of humpback whale song. Philos. Trans. R. Soc. B 376, 20200242 (2021).Article 

    Google Scholar 
    Crates, R. et al. Loss of vocal culture and fitness costs in a critically endangered songbird. Proc. R. Soc. B 288, 20210225 (2021).Article 

    Google Scholar 
    Garland, E. C., Garrigue, C. & Noad, M. J. When does cultural evolution become cumulative culture? A case study of humpback whale song. Philos. Trans. R. Soc. B 377, 20200313 (2022).Article 

    Google Scholar 
    Garland, E. C. et al. Improved versions of the Levenshtein distance method for comparing sequence information in animals’ vocalisations: tests using humpback whale song. Behaviour 149, 1413–1441 (2012).Article 

    Google Scholar 
    Garland, E. C. et al. The devil is in the detail: quantifying vocal variation in a complex, multileveled, and rapidly evolving display. J. Acoust. Soc. Am. 142, 460–472 (2017).ADS 
    Article 

    Google Scholar 
    Rekdahl, M. L. et al. Culturally transmitted song exchange between humpback whales (Megaptera novaeangliae) in the southeast Atlantic and southwest Indian Ocean basins. R. Soc. Open Sci. 5, 172305 (2018).ADS 
    Article 

    Google Scholar 
    Suzuki, R. & Shimodaira, H. Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22, 1540–1542 (2006).CAS 
    Article 

    Google Scholar 
    Sokal, R. R. & Rohlf, F. J. The comparison of dendrograms by objective methods. Taxon 11(2), 33–40 (1962).Article 

    Google Scholar 
    R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2015. URL http (R Core Development Team, 2016). More

  • in

    Future reversal of warming-enhanced vegetation productivity in the Northern Hemisphere

    Friedlingstein, P. et al. Global carbon budget 2020. Earth Syst. Sci. Data 12, 3269–3340 (2020).
    Google Scholar 
    Myneni, R. B. et al. A large carbon sink in the woody biomass of northern forests. Proc. Natl Acad. Sci. USA 98, 14784–14789 (2001).CAS 

    Google Scholar 
    Sitch, S. et al. Recent trends and drivers of regional sources and sinks of carbon dioxide. Biogeosciences 12, 653–679 (2015).
    Google Scholar 
    Kauppi, P. E. et al. Large impacts of climatic warming on growth of boreal forests since 1960. PLoS ONE 9, e111340 (2014).
    Google Scholar 
    Zhu, Z. C. et al. Greening of the Earth and its drivers. Nat. Clim. Change 6, 791–795 (2016).CAS 

    Google Scholar 
    Piao, S. L. et al. Characteristics, drivers and feedbacks of global greening. Nat. Rev. Earth Environ. 1, 14–27 (2020).
    Google Scholar 
    IPCC Climate Change 2013: The Physical Science Basis (eds Stocker, T. F. et al.) (Cambridge Univ. Press, 2013).Penuelas, J. et al. Shifting from a fertilization-dominated to warming-dominated period. Nat. Ecol. Evol. 1, 1438–1445 (2017).
    Google Scholar 
    D’Arrigo, R., Wilson, R., Liepert, B. & Cherubini, P. On the ‘divergence problem’ in northern forests: a review of the tree-ring evidence and possible causes. Glob. Planet. Change 60, 289–305 (2008).
    Google Scholar 
    Beck, P. S. A. et al. Changes in forest productivity across Alaska consistent with biome shift. Ecol. Lett. 14, 373–379 (2011).
    Google Scholar 
    Vickers, H. et al. Changes in greening in the High Arctic: insights from a 30-year AVHRR max NDVI dataset for Svalbard. Environ. Res. Lett. 11, 105004 (2016).
    Google Scholar 
    Piao, S. L. et al. Evidence for a weakening relationship between interannual temperature variability and northern vegetation activity. Nat. Commun. 5, 5018 (2014).CAS 

    Google Scholar 
    Duffy, K. A. et al. How close are we to the temperature tipping point of the terrestrial biosphere? Sci. Adv. 7, eaay1052 (2021).CAS 

    Google Scholar 
    Liu, Y. W. et al. Seasonal responses of terrestrial carbon cycle to climate variations in CMIP5 models: evaluation and projection. J. Clim. 30, 6481–6503 (2017).
    Google Scholar 
    Huang, M. T. et al. Air temperature optima of vegetation productivity across global biomes. Nat. Ecol. Evol. 3, 772–779 (2019).
    Google Scholar 
    Park, T. et al. Changes in timing of seasonal peak photosynthetic activity in northern ecosystems. Glob. Change Biol. 25, 2382–2395 (2019).
    Google Scholar 
    Keeling, C. D., Chin, J. F. S. & Whorf, T. P. Increased activity of northern vegetation inferred from atmospheric CO2 measurements. Nature 382, 146–149 (1996).CAS 

    Google Scholar 
    Piao, S. L., Friedlingstein, P., Ciais, P., Viovy, N. & Demarty, J. Growing season extension and its impact on terrestrial carbon cycle in the Northern Hemisphere over the past 2 decades. Glob. Biogeochem. Cycles 3, GB3018 (2007).
    Google Scholar 
    Keenan, T. F. et al. Net carbon uptake has increased through warming-induced changes in temperate forest phenology. Nat. Clim. Change 4, 598–604 (2014).CAS 

    Google Scholar 
    Xia, J. Y. et al. Joint control of terrestrial gross primary productivity by plant phenology and physiology. Proc. Natl Acad. Sci. USA 112, 2788–2793 (2015).CAS 

    Google Scholar 
    Eyring, V. et al. Overview of the Coupled Model Intercomparison Project Phase 6 (CMIP6) experimental design and organization. Geosci. Model Dev. 9, 1937–1958 (2016).
    Google Scholar 
    Meehl, G. A. & Tebaldi, C. More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305, 994–997 (2004).CAS 

    Google Scholar 
    Yamori, W., Hikosaka, K. & Way, D. A. Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation. Photosynth. Res. 119, 101–117 (2014).CAS 

    Google Scholar 
    Berry, J. & Bjorkman, O. Photosynthetic response and adaptation to temperature in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 31, 491–543 (1980).
    Google Scholar 
    Chen, A., Huang, L., Liu, Q. & Piao, S. L. Optimal temperature of vegetation productivity and its linkage with climate and elevation on the Tibetan Plateau. Glob. Change Biol. 27, 1942–1951 (2021).
    Google Scholar 
    Smith, N. G., Lombardozzi, D., Tawfik, A., Bonan, G. & Dukes, J. S. Biophysical consequences of photosynthetic temperature acclimation for climate. J. Adv. Model. Earth Syst. 9, 536–547 (2017).
    Google Scholar 
    Chen, M. & Zhuang, Q. L. Modelling temperature acclimation effects on the carbon dynamics of forest ecosystems in the conterminous United States. Tellus B 65, 19156 (2013).
    Google Scholar 
    Crous, K. Y. Plant responses to climate warming: physiological adjustments and implications for plant functioning in a future, warmer world. Botany 106, 1049–1051 (2019).
    Google Scholar 
    Conley, M. M. et al. CO2 enrichment increases water-use efficiency in sorghum. New Phytol. 151, 407–412 (2001).
    Google Scholar 
    Norby, R. J. & Zak, D. R. Ecological lessons from free-air CO2 enrichment (FACE) experiments. Annu. Rev. Ecol. Evol. Syst. 42, 181–203 (2011).
    Google Scholar 
    Huang, M. T. et al. Change in terrestrial ecosystem water-use efficiency over the last three decades. Glob. Change Biol. 21, 2366–2378 (2015).
    Google Scholar 
    Gonsamo, A. et al. Greening drylands despite warming consistent with carbon dioxide fertilization effect. Glob. Change Biol. 7, 3336–3349 (2021).
    Google Scholar 
    Keenan, T. F. et al. Increase in forest water-use efficiency as atmospheric carbon dioxide concentrations rise. Nature 499, 324–327 (2013).CAS 

    Google Scholar 
    Lemordant, L. et al. Modification of land–atmosphere interactions by CO2 effects: implications for summer dryness and heat wave amplitude. Geophys. Res. Lett. 43, 10240–10248 (2016).CAS 

    Google Scholar 
    Lian, X. et al. Summer soil drying exacerbated by earlier spring greening of northern vegetation. Sci. Adv. 6, eaax0255 (2020).
    Google Scholar 
    Lian, X. et al. Multifaceted characteristics of dryland aridity changes in a warming world. Nat. Rev. Earth Environ. 4, 232–250 (2021).
    Google Scholar 
    Druel, A., Ciais, P., Krinner, G. & Peylin, P. Modeling the vegetation dynamics of northern shrubs and mosses in the ORCHIDEE land surface model. J. Adv. Model. Earth Syst. 11, 2020–2035 (2019).
    Google Scholar 
    Scheiter, S., Langan, L. & Higgins, S. I. Next-generation dynamic global vegetation models: learning from community ecology. New Phytol. 198, 957–969 (2013).
    Google Scholar 
    Mod, H. K. & Luoto, M. Arctic shrubification mediates the impacts of warming climate on changes to tundra vegetation. Environ. Res. Lett. 12, 124028 (2016).
    Google Scholar 
    Zhang, Y., Commane, R., Zhou, S., Williams, A. P. & Gentine, P. Light limitation regulates the response of autumn terrestrial carbon uptake to warming. Nat. Clim. Change 10, 739–743 (2020).CAS 

    Google Scholar 
    Bauerle, W. L. et al. Photoperiodic regulation of the seasonal pattern of photosynthetic capacity and the implications for carbon cycling. Proc. Natl Acad. Sci. USA 109, 8612–8617 (2012).CAS 

    Google Scholar 
    Zhang, Y., Parazoo, N. C., Williams, A. P., Zhou, S. & Gentine, P. Large and projected strengthening moisture limitation on end-of-season photosynthesis. Proc. Natl Acad. Sci. USA 117, 9216–9222 (2020).CAS 

    Google Scholar 
    Fritz, M. et al. Brief communication: future avenues for permafrost science from the perspective of early career researchers. Cryosphere 9, 1715–1720 (2015).
    Google Scholar 
    Jin, X. Y. et al. Impacts of climate-induced permafrost degradation on vegetation: a review. Adv. Clim. Change Res. 12, 29–47 (2021).
    Google Scholar 
    Tramontana, G. et al. Predicting carbon dioxide and energy fluxes across global FLUXNET sites with regression algorithms. Biogeosciences 13, 4291–4313 (2016).CAS 

    Google Scholar 
    Zhang, Y., Joiner, J., Alemohammad, S. H., Zhou, S. & Gentine, P. A global spatially contiguous solar-induced fluorescence (CSIF) dataset using neural networks. Biogeosciences 15, 5779–5800 (2018).CAS 

    Google Scholar 
    Navarro-Racines, C., Tarapues, J., Thornton, P., Jarvis, A. & Ramirez-Villegas, J. High-resolution and bias-corrected CMIP5 projections for climate change impact assessments. Sci. Data 7, 7 (2020).
    Google Scholar  More

  • in

    Regional asymmetry in the response of global vegetation growth to springtime compound climate events

    Illustration of the compound event indicesBuilding on earlier studies24,25, we develop two univariate indices to model concurrent climate conditions, i.e., a CWD index that varies from compound cold-wet conditions to CWD conditions, and a CCD index that varies from compound warm-wet conditions to CCD conditions (see “Methods”). The two indices incorporate the dependence between temperature and precipitation and are a measure of how warm/cold and dry a point is relative to the distribution of climate conditions at a given location. We illustrate the two indices on two grid points that have strong but opposite temperature-precipitation correlation. In the case where temperature and precipitation are strongly negatively correlated, the CWD index is well aligned with the primary axis of the bivariate distribution (Fig. 1a). In the case where temperature and precipitation are strongly positively correlated, the same holds for the CCD index (Fig. 1d). As illustrated for several concurrent hot-dry and cold-dry events that occurred around the globe, the two indices well capture these events (Supplementary Figs. 1 and 2).Fig. 1: The relationship between precipitation and temperature and compound indices.a Scatter plot of summer precipitation and temperature anomalies (z-score) with corresponding CWD index in color (see “Methods”). The location is at 97.25°W and 33.75°N from 1901 to 2018. b The same as a but for spring at 84.75°E and 66.75°N. c Same distribution as in a but colored based on the CCD index. d Same distribution as in b but colored based on the CCD index.Full size imageNotably, in the case where precipitation and temperature are strongly positively correlated, the CWD index indicates the relative anomalies of bivariate joint distribution, and some counterintuitive situations might occur relative to the univariate marginals (Fig. 1b). For instance, points might be labeled as strong CWD events (CWD index > 1.5) even though temperature is anomalously cold (temperature anomalies < 0, red dots in lower left quadrant of Fig. 1b). The CCD index exhibits similar behavior (Fig. 1c). This indicates an interesting property of the compound indices to identify strong compound conditions relative to bivariate distribution that are not necessarily extreme from a univariate perspective3,24,26,27.Widespread direct and lagged impacts of springtime compound climate conditionsTo evaluate the lagged summer vegetation responses to spring compound climate conditions, we compute partial correlation between CWD (CCD) spring and subsequent summer vegetation variation by controlling for the influence of summer compound climate conditions on these correlations (see “Methods”). Results show widespread negative associations between CWD spring and subsequent summer vegetation in the mid-latitudes (50°N).a–c The average standardized anomalies (z-score) of GPP during CWD spring but subsequent non-CWD summer (a), non-CWD spring but subsequent CWD summer (b), and consecutive CWD spring and summer (c) for areas in Fig. 2a where summer vegetation responds positively (r ≥ 0.22) to spring CWD climate conditions. d–f The same as a–c, but for soil moisture. g–i The same as a–c, but for runoff. The bar plots with dash lines (without dash line) indicate the average anomalies of multiple observation-based (model-based) products, and the circles indicate the average anomalies of each product. GLASS, LUE, NIRv, Flux-CRU, and Flux-ERA5 are observation-based GPP products, while model simulations are taken from TRENDYv6. GLEAM is observation-based soil moisture. GRUN represents observation-based runoff. GLDAS-VIC, GLDAS-Noah, GLDAS-Catchment, and FLDAS indicate assimilatory soil moisture and runoff that incorporate satellite- and ground-based observational products.Full size imageFig. 4: The responses of vegetation productivity and hydrological variables to CWD events in mid-latitudes (23.5–50°N/S).a–c The average standardized anomalies (z-score) of GPP during CWD spring but subsequent non-CWD summer (a), non-CWD spring but subsequent CWD summer (b), and consecutive CWD spring and summer (c) for areas in Fig. 2a where summer vegetation responds negatively (r ≤ −0.22) to spring CWD climate conditions. d–f The same as a–c, but for soil moisture. g–i The same as a–c, but for runoff. The bar plots with dash lines (without dash line) indicate the average anomalies of multiple observation-based (model-based) products, and the circles indicate the average anomalies of each product. For details on data see Fig. 3.Full size imageFig. 5: The effects of CCD events on vegetation productivity and hydrological variables in mid-to-high latitudes.a–c The average standardized anomalies (z-score) of GPP during CCD spring but subsequent non-CCD summer (a), non-CCD spring but subsequent CCD summer (b), and consecutive CCD spring and summer (c) for areas in Fig. 2b where summer vegetation responds negatively (r ≤ −0.22) to spring CCD climate conditions. d–f The same as a–c, but for soil moisture. g–i The same as a–c, but for runoff. The bar plots with dash lines (without dash line) indicate the average anomalies of multiple observation-based (model-based) products, and the circles indicate the average anomalies of each product. For details on data see Fig. 3.Full size imageCWD events increase vegetation productivity in high latitudesWe first analyze the direct responses of productivity to springtime and summertime CWD events across high latitudes ( >50°N, Fig. 3). Productivity increases during CWD spring and summer (Fig. 3a–c), which is consistent with vegetation responses (Supplementary Fig. 8a–c). Despite elevated spring greenness, spring water overall shows positive anomalies during CWD spring (Fig. 3d, f, g, i). This result indicates that spring greenness during CWD conditions is not associated with dry spring across high latitudes, which is further confirmed by similar anomalies in springtime TWS (Supplementary Fig. 8d, f). In contrast, severe water reduction is found in CWD summer (Fig. 3e, f, h, i). This suggests that despite the beneficial effects of CWD events on productivity in summer, they are associated with summer water deficit.Next, to analyze the lagged effects of springtime CWD events, we investigate the productivity anomalies in summer under three cases, namely CWD spring but non-CWD summer, non-CWD spring but CWD summer, and consecutive CWD spring and summer. Our results indicate that springtime CWD events have positive lagged effects on summer productivity across high latitudes (Fig. 3). Specifically, we find that during non-CWD summer (that is not favorable for summer vegetation growth) preceded by CWD spring, positive anomalies are still found in summer productivity (Fig. 3a). In contrast, during CWD summer (preceded by non-CWD spring), some models and observation-based products exhibit a reduction in summer productivity (Fig. 3b). We further find that summer productivity highly increases during consecutive events (Fig. 3c). Vegetation anomalies show similar behaviors (Supplementary Fig. 8a–c). Regarding the lagged responses of hydrological variables, CWD springs followed by non-CWD summers do not lead to water dryness, despite increased vegetation greenness (Fig. 3d, g). The magnitude of summer water deficit is similar for both cases that include CWD summer (Fig. 3e, f, h, i) and is consistent with summer TWS anomalies (Supplementary Fig. 8e, f). These results imply that in high latitudes, summer water reductions characterized by TWS, soil moisture, and runoff are not associated with increased spring greenness but are primarily caused by summer precipitation deficit.The productivity responses to compound climate conditions may be stronger than that to individual events through the synergistic effects of temperature and precipitation28. To investigate this, we compute the average anomalies in GPP and soil moisture associated with univariate events across the focus areas, which are then compared with the effects of CWD and CCD events in high latitudes (see “Methods”). Warm events can not only directly increase productivity but also show positive lagged effects (Supplementary Fig. 9a, b). In contrast, dry events reduce productivity (Supplementary Fig. 9e, f). This indicates that the direct and lagged positive effects of CWD events across high latitudes are mainly dominated by the warm component, while dry conditions have negative effects. Therefore, the warm-induced increase in productivity slightly exceeds that associated with CWD events (Supplementary Fig. 9b). Soil moisture under warm springs shows positive anomalies (Supplementary Fig. 9c, d), while they slightly decline during dry spring (Supplementary Fig. 9g, h). This suggests that the positive anomalies in soil water during CWD spring are driven by the warm component.CWD events reduce vegetation productivity in mid-latitudesHere, we first investigate the direct effects of springtime and summertime CWD events across mid-latitudes (23.5–50°N/S). Springtime productivity exhibits little changes during CWD spring (Fig. 4a, c), despite dry spring (Fig. 4d, f, g, i). When considering the direct effects of CWD events in summer, the results are similar, whereas the negative magnitude of productivity in summer is larger than that in spring (Fig. 4b, c). This difference suggests CWD conditions in summer show more adverse effects on productivity than that in spring in mid-latitudes. The anomalies in vegetation and TWS are consistent (Supplementary Fig. 10).Next, the lagged effects of springtime CWD events in mid-latitudes are assessed. In cases with CWD spring but non-CWD summer, summer productivity exhibits slight anomalies (Fig. 4a), with slightly decreased summer water (Fig. 4d, g). Summer productivity and water show much higher reductions in case with consecutive events (Fig. 4c, f, i) than for the case with only CWD summer (Fig. 4b, e, h). These results are supported by the responses of vegetation indices and TWS (Supplementary Fig. 10), revealing that springtime CWD events in mid-latitudes have negative lagged effects on summer productivity and water availability.The direct and lagged effects of individual events are finally compared with that of CWD events in mid-latitudes. Dry conditions in spring and summer directly decrease productivity and cause soil water dryness (Supplementary Fig. 11a–d). Moreover, dry spring depletes soil moisture earlier, which, in turn, causes dry summer and reduction in productivity during non-dry summer (Supplementary Fig. 11a, c). This indicates that dry springs have negative lagged effects on summer productivity. In contrast, productivity and soil water show positive anomalies during warm springs, while they show negative anomalies in summer (Supplementary Fig. 11e–h). These results suggest that the direct and lagged negative effects of CWD springs are dominated by the dry component in mid-latitudes, while the warm component mitigates the negative effects of the dry component in spring. Accordingly, the decline in productivity due to dry conditions thus exceeds that triggered by CWD events (Supplementary Fig. 11b).Decreased vegetation productivity due to the negative synergistic effects of CCD eventsHere, we first investigate the direct effects of CCD events across mid-to-high latitudes. Productivity reductions are found during springtime and summertime CCD events (Fig. 5a–c) concurrent with water reductions (Fig. 5). Vegetation and TWS show similar behaviors during CCD spring and summer (Supplementary Fig. 12). These results reveal that CCD events in spring and summer can impose direct adverse impacts on productivity and soil water across mid-to-high latitudes. The productivity reductions in spring and summer are similar in magnitude (Fig. 5a, b), indicating that CCD events between spring and summer can cause similar damage to productivity.We then analyze the lagged effects of springtime CCD events. Our results indicate that springtime CCD events show negative lagged effects on summer productivity and cause summer water reductions in mid-to-high latitudes (Fig. 5). Specifically, we find that in cases with CCD spring but non-CCD summer, summer productivity and water exhibit strongly negative anomalies (Fig. 5a, d, g). Moreover, summer anomalies are higher during consecutive events (Fig. 5c, f, i) than the cases including only CCD summer (Fig. 5b, e, h). Vegetation indices and TWS show similar responses (Supplementary Fig. 12). Our results further indicate that CCD spring has more severe negative lagged effects on productivity than CWD spring. That is, we find that in comparison to cases with preceding CWD spring and consecutive CWD events, summer productivity shows higher reduction in cases with preceding CCD spring and consecutive CCD events (Fig. 4a, c versus Fig. 5a, c). Moreover, in cases with CCD spring but non-CCD summer (Fig. 5a, d, g), summer anomalies are close to those in scenarios with non-CCD spring but CCD summer (Fig. 5b, e, h). The vegetation and TWS anomalies further confirm this situation (Supplementary Fig. 12a, b, d, e). These results suggest that the lagged effects of CCD spring can be of similar magnitude as their direct adverse effects.We finally compare the direct and lagged effects of individual events with that of CCD events in mid-to-high latitudes. Cold conditions in spring and summer directly reduce productivity but show weak effects on soil moisture (Supplementary Fig. 13a–d), and cold spring shows negative lagged effects on summer productivity (Supplementary Fig. 13a). Dry events show direct and lagged negative effects on productivity and soil moisture (Supplementary Fig. 13e–h). These results imply that the negative lagged effects of CCD springs are dominated by both cold and dry components. The effects of CCD events on productivity mostly exceeds the individual dry or cold impacts (Supplementary Fig. 13a, b, e, f). More

  • in

    California wildfire spread derived using VIIRS satellite observations and an object-based tracking system

    OverviewIn this study, we used VIIRS active fire detections to track the dynamic evolution of all fires in California from 2012 to 2020 (Fig. 1). We developed an approach that has the following steps. First, after reading the satellite fire pixel data at each 12-hour time step, the new fire pixels are aggregated into multiple clusters using the fire pixel locations and an automatic clustering algorithm. These clusters are then spatially compared to existing fire objects. If a cluster is not close to any existing active fire object, we use all fire pixels within the cluster to form a new fire object. If a cluster is located near an existing fire object which is still active, we view the cluster as an extension of the existing fire. In this case, we append all pixels within the cluster to the corresponding existing fire object, allowing the existing object to grow. When a fire expands and gets close enough (within a pre-defined distance threshold) to an existing active fire object, we merge the two objects. For each time step (12 hours in this case for the two overpasses), we derive or update a suite of attributes and status indicators associated with each fire event, including pixel-level attributes of fire and surface properties, vector geometries related to the fire shape, and meta-attributes characterizing the entire fire object.Data inputSatellite remote sensing instruments provide active fire detections with accurate geographical location and broad spatial coverage. The primary data for this fire tracking system are active fire locations and the fire radiative power (FRP) recorded by the VIIRS instrument aboard the Suomi National Polar-orbiting Partnership (Suomi-NPP) satellite24. VIIRS observes Earth’s surface twice each day in low and mid latitude regions, with local overpass times of approximately 1:30 am and 1:30 pm. Compared to its predecessor, the MODIS sensors on the Terra and Aqua satellites, VIIRS has a higher spatial resolution and can detect smaller and cooler fires24. Also, the VIIRS instrument provides a more consistent pixel area across the image swath25, resulting in more accurate estimates of active fire location. Therefore, compared with MODIS, the VIIRS active fire products can be used to map fire event progression with higher accuracy21. Two streams of VIIRS active fire data are operationally produced using a contextual fire detection algorithm24, drawing upon VIIRS moderate resolution band (M-band) and imaging band (I-band) reflectance and radiance data layers. In this fire tracking system, we used the Suomi-NPP VIIRS I-band fire location data product (VNP14IMGML, Collection 1 Version 4) that contains the centre location, FRP, scan angle, and other attribute fields associated with each pixel. The I-band fire detection product has a 375-m spatial resolution at nadir (the sub-satellite point) and an average resolution across the full swath of about 470 m. Theoretical estimates of fire detection efficiency for the VIIRS sensor indicate that during the day, VIIRS can detect 700 K fires with 50% probability that have a size of about 200 m2 (a 15 m × 15 m fire area)24. During night, the detection efficiency increases, and VIIRS can detect 700 K fires as small as 40 m2. From a fire spread tracking perspective, these detection efficiencies imply that in many instances, the area of a fire pixel that is covered with flaming fire combustion is several orders of magnitude smaller than the overall pixel size. The VNP14IMGML data, available from 2012 onwards, were downloaded from the University of Maryland VIIRS Active Fire website (https://viirsfire.geog.umd.edu/).Land cover data are an additional input in the system required to classify different fire types and determine the spatial connectivity threshold. Here we use the U.S. National Land Cover Database (NLCD 2016)26 that is available from the Multi-Resolution Land Characteristics (MRLC) Consortium website (https://www.mrlc.gov/national-land-cover-database-nlcd-2016). We aggregated the original 30-m data to match the spatial resolution of VIIRS active fire data, and merged the original 16 classes into several groups: ‘Water’, ‘Urban’, ‘Barren’, ‘Forest’, ‘Shrub’, ‘Grassland’, and ‘Agriculture’. We used the 1000-hour dead fuel moisture from the high-resolution (4 km) gridMET product27 for the purpose of separating wildfires and management fires. This gridMET dataset was computed from 7–day average conditions composed of day length, hours of rain, and daily temperature and humidity ranges. Regularly updated gridMET data are available from the Climatology Lab website (http://www.climatologylab.org/gridmet.html).Other ancillary and validation datasets used in this study included a shapefile of California borders and fire perimeters from the California Forestry and Fire Protection’s Fire and Resource Assessment Program (FRAP) dataset (https://frap.fire.ca.gov/mapping/maps/).Fire object hierarchyFire detections from VIIRS are dynamically tracked within the framework of a three-level object hierarchy (Fig. 1). The lowest level is the fire pixel object, which includes the geographical location (latitude and longitude), the FRP value, and the origin (first assigned fire object id). The second level is the fire object, which includes all attributes associated with each individual fire event at a particular time step (Table 2). Each fire object includes one or more fire pixel objects, a unique identification number (id), and a set of attributes associated with the whole fire. Two types of fire attributes are derived and recorded for each fire object. The first type encompasses temporal (e.g., ignition time, duration) and spatial (e.g., centroid, ignition location) characteristics of the object as well as general properties (e.g., size, type, active status). The second type is the geometric information related to the fire object, including the fire perimeter, the active fire front line, and the newly detected fire pixel locations (stored as vectors). All fire objects in the State of California are combined to form an allfires object, to characterize the whole-region fire situation at a specific time step. The allfires object comprises a list of fire objects, and also contains meta information representing the statistics of all fires and the records describing fire evolution. A full list of the attributes associated with the pixel object, the fire object, and the allfires object is presented in Table 2.Table 2 List of main attributes associated with pixel, fire and allfires objects.Full size tableFire event trackingThe fire records (locations and FRPs) from the monthly VIIRS active fire location products (VNP14IMGML) are read into the system at each half-daily time step (roughly 1:30 am and 1:30 pm local time). We apply spatial and temporal filters to the data to extract active fire pixels recorded in California during each 12-hour time interval. We also apply quality flag filters (thermal anomaly type of ‘0: presumed vegetation fire’ in VNP14IMGML)) to ensure the use of only pixels likely associated with vegetation fires. The fire location and FRP values are used to create fire pixel objects. To speed up the calculation, the newly detected active fire pixels after filtering are first aggregated to specific clusters using the distances between them and an automatic clustering algorithm. In this initial aggregation algorithm, a ball tree28 is created to partition all newly detected active fire pixels into a nested set of hyperspheres in a 2-D space (latitude and longitude). This space partitioning data structure can be used to expedite nearest neighbours search29 and allow for quick cluster grouping. Here we refer to a cluster as a collection of pixel objects that are recorded at the same time step and are also spatially nearby. In the following steps, all pixels within a cluster are considered as a whole for fire merging and creation.We define an extended area for every existing fire object as the fire vector perimeter (see the section of Calculating and recording fire attributes for detail) plus a radial buffer that depends on the fire type property of the object. The buffer is set to 5 km for forest fires and 1 km for other fire types (shrub, crop, urban), considering that the fire spread rate can differ across biomes13. We then evaluate the spatial distance between the perimeters of a newly classified cluster and all existing active fire objects (a fire object keeps an active status if one or more active fire pixels associated with it are detected during the past 5 days), and calculate the shortest distance. If the shortest distance is smaller than the buffer of the associated existing active fire (i.e., new cluster overlaps with the extended area of an existing fire object), we assume all fire pixels in the new cluster are associated with the growth of the existing fire object at the current time step (Fig. 2). The existing fire object is updated by appending all fire pixel objects within the new cluster. If a newly classified cluster does not overlap with the extended area of any existing active fire object, we assume this is a new fire. A new fire object (by assigning a new fire id) is created using all fire pixel objects in the cluster.With the addition of new fire pixels, an existing fire object may expand and touch the extended area of another existing active fire object. If this happens, we assume that these two existing fire objects merge into a single object at this time step. All fire pixels in the fire object with a higher id number (a later start date, termed as the ‘source fire’) are appended to the fire object with lower id number (earlier start date, termed as the ‘target fire’) in this case. We record the id of the target fire in a list of fire mergers, and update all attributes associated with this fire (Fig. 3). In order to avoid double counting, the source fire object (with all pixels being transferred to the target fire object) is flagged as invalid, and is excluded from statistical analysis of fire events.Fig. 3The time series of growth for the SCU Lightning Complex fire (2020). Panel (b) shows the fire size of the SCU fire (total area within the fire object perimeter) at half-daily time steps. A fraction of the fire growth (shown in orange) was due to the addition of newly detected fire pixels. Panel (a) shows the number of new fire pixels (associated with the SCU fire object) detected at each time step. The other part of the fire growth (shown in red) was due to the merging with existing fire objects. Panel (c) shows the number of fire pixels in the existing objects that were merged to the SCU fire object.Full size imageCalculating and recording fire attributesOther than individual fire pixels contained in a fire object, several core attributes (properties and geometries) are also dynamically updated at each time step and are used for fire tracking and characterization.Important time-related attributes include the fire ignition time (the time step at which the first fire pixel within the fire object was detected), the fire end time (the latest time step with an active fire observation), and the fire duration (the time difference between the ignition time and end time). If a fire object does not have new active fire pixels appended during 5 consecutive days (i.e., the fire end time is more than 5 days before the present time step), its status is set to inactive. Once inactive, a fire object is no longer evaluated for use in future clustering (i.e., new active fire detections later will form new fire objects, even if they are spatially close to the inactive fire object).Each fire object is assigned to a specific fire type. The fire type is identified using the major land cover type within the fire perimeter (Table 3). In an initial analysis, we found that prescribed fires, on average, have higher coarse fuel moisture levels than wildfires. Therefore, we also record the 1000-hour fuel moisture (fm1000) from the gridMET dataset27 for each fire object (corresponding to the ignition time step) and use this value to divide forest and shrub fires further to wildfire and prescribed types.Table 3 Classification of fire types based on dominant land cover type (from the US National Land Cover Database) within each fire perimeter and the 1000-hr fuel moisture (FM-1000, from gridMET dataset) at the time of ignition.Full size tableAn essential step in this object-based fire tracking system is to determine the vector shape of the fire perimeter. In this system, we use an alpha shape30 algorithm to derive bounding polygons containing fire pixels in a fire object. For an alpha shape, the radius of the disks forming the curves in the polygon is determined by the alpha parameter α. Compared with the commonly used convex hull, the alpha shape hull is able to capture the irregular shapes around the fire perimeter more accurately22.To identify the optimal values for the α parameter, we performed the following analysis. First, we derived the final fire perimeters for all large fires that occurred in California during the 2018 wildfire season using a set of α values ranging from 500 m to 10 km and compared the results with more refined fire perimeters from the Fire and Resource Assessment Program (FRAP) dataset (Fig. 4). Large magnitude α values tended to overestimate the total burned area, while small α values often fragmented a large fire event. We found that a value of α = 1 km was optimal in terms of balancing the ability of the hull to catch the boundary shape and to keep the integrity of a fire object. For each time step, we applied the alpha shape algorithm to all fire pixel locations associated with a fire object since the time of ignition. This processing step resulted in a concave hull with the shape of polygon or multipolygon. To account for the pixel size, we expanded the concave hull to the fire perimeter using a buffer size equal to half of the VIIRS nadir cross-track pixel width (187.5 m). The alpha shape algorithm does not work when the total number of fire pixels (npix) is less than 4. If npix equals 3, we used a convex hull algorithm and the same 187.5 m buffer to determine a polygon perimeter. If npix is 1 or 2, circles centered on the fire pixel location with radius of 187.5 m were used.Fig. 4Optimization of the alpha shape parameter (α). For all large fires (final size  > 4 km2) in California during 2018, fire perimeters were estimated using VIIRS active fires and different alpha parameters. By comparing (a) the burned area (BA) and (b) the number of fire objects with the FRAP data, an optimal alpha parameter of 1 km was identified for use in this study (shown in red). The vertical bars and lines show the mean and 1-std variability from all fires. The dashed blue lines indicate the ideal values when compared to FRAP. Panels (c)–(h) show the fire perimeters derived using different alpha shape parameters for two sample fires in 2018. The shapes with pink color are final FEDS fire perimeters derived from VIIRS active fires using the alpha shape algorithm. The blue shapes represent the corresponding fire perimeters from the FRAP dataset. Overlap between FRAP and FEDS is shown in purple.Full size imageWe also calculate the active front line for each fire object at each time step. The active fire front consists of the segments of the fire perimeter that are actively burning and releasing energy and emissions. The position of the active fire line is critical in evaluating the fire risk, estimating the fire emissions, and predicting fire spread. We derive the active portion of the fire perimeter as segments that are within a 500 m radius of newly detected fire pixel locations. We found that this threshold allowed for a continuous projection of the active fire front in rapidly expanding areas of large wildfires during the 2018 fire season; this threshold may be optimized in future work to maximize performance metrics for fire model forecasts. The resulting active line for each fire at each time step has the shape of a linestring (object representing a sequence of points and the line segments connecting them), a multi-linestring (a collection of multiple linestrings), or a linear ring (closed linestring). Figure 5 shows an example map of the fire perimeters and active fire front lines on September 8 during the 2020 wildfire season.Fig. 5An example map of fire perimeters and fire active fronts in California. The map was created using the fire event data suite (FEDS) as of the Suomi-NPP afternoon overpass (~1:30 pm local time) of Sep 8, 2020. The background is the Aqua MODIS Corrected Reflectance Imagery (true color) recorded at the same day (provided by the NASA Global Imagery Browse Services). The active front line of a fire is shown in yellow, active fire areas are shown in red, and the area of inactive (extinguished) fires are shown in dark red.Full size imageAdditional fire properties, such as the fire area and active fire line length, are also derived using these geometries of the fire object (see Table 2). Note this list can be easily expanded to include more user-defined properties with the help of the fire object core vector data.The allfires object contains a list of all existing fire objects at a time step. This object also records the ids of fire objects that have been modified (including fires newly formed, fires that expanded with new pixel additions, fires with pixels addition due to merging, and fires that just became invalid) at the current time step.Creating the fire event data suite (FEDS)By tracking the spatiotemporal evolution of all fire objects in California, we derived a complete dataset of fire events for each calendar year (Jan 1 am – Dec 31 pm) during the Suomi-NPP VIIRS era (2012–2020). The dataset contains four products that represent the fire information in California at multiple spatial scales and from different perspectives (Fig. 1 and Table 4), ranging from the most detailed and memory-intensive data format (Pickle) to the most high-level format (CSV).Table 4 Data structure of the FEDS.Full size tableThe first product is the direct serialization result of the allfires object at each time step (twice per day). The product is stored as a Pickle file31 which allows for analysis of the complex allfires object structure (including all attributes associated with all fire objects it contains). This file also serves as the restart file for continued fire tracking at any time step, which is essential for the operational mode using the near-real-time fire data. By restoring an exact copy of the previously pickled allfires object, any attribute in the allfires object can be deserialized from the saved files. The Pickle file is the most basic data product in the dataset, and is created at each half-day time step.The second product (Snapshot) represents a more accessible and self-explanatory variant of the Pickle serialization product. In this product, we tabulated important diagnostic attributes for each fire and saved them in GeoPackage32 data files. Each GeoPackage file includes three data layers: one contains the properties and the fire perimeter geometry, another contains the active fire line geometry, and a third contains the new fire pixel location geometry. This product, created at a half-daily time step, allows for a more straightforward interpretation of regional fire status at a particular time step. We also created a GeoPackage file that summarizes the final fire perimeters and attributes for all fires during the whole study period (2012–2020).The third product (Largefire) focuses on the temporal evolution of individual large fires with an area greater than 4 km2. At each time step, the time series of properties and geometries (fire perimeter, active fire line, and new fire pixel locations) for each of the large fires are extracted and saved to GeoPackage files. This product facilitates the visualization and analysis for an individual targeted fire (Fig. 6) and is particularly useful in the near-real-time evaluation, forecasting, and policy making.Fig. 6The spatiotemporal evolution of the Creek fire (2020). Contours and dots reflect the fire perimeters and newly detected fire pixels at each 12-hour time step. Data for the period of Sep 5 am–Nov 6 am, 2020 are shown.Full size imageThe fourth product (Summary), which is stored as NetCDF and CSV files and created at the end of a fire season, records the all-year time series of fire statistics (including major fire attributes such as number, size, duration, fire line length, etc.) over the whole State of California. This product provides a feasible regional summary of the temporal evolution of fires.Potential for near-real-time (NRT) fire event trackingWhile the main objective of this paper is to apply the object-based fire tracking system to historical VIIRS fire detections and create a retrospective multi-year FEDS, we note that this system has the potential to be used for tracking fire events in near-real-time, providing rich and valuable information for fire management and short-term risk assessment. We have experimented with the use of this system for NRT fire event tracking in California using the daily NRT Suomi-NPP VIIRS active fire detection product (VNP14IMGTDL, collection 6) as the main data source. The VNP14IMGTDL product is routinely produced and is publicly available at the NASA Fire Information for Resource Management System (FIRMS). Since the NRT product undergoes less rigorous quality assurance, we use only fires with ‘nominal’ or ‘high’ confidence levels from the NRT product for fire tracking. Some active fire detections from the NRT data are potentially associated with static non-vegetation fires (e.g., fires from gas flaring in oil and gas or landfill industries or false detections due to reflection from solar panels) and are not the main interest for vegetation fire studies. To avoid the unnecessary computation associated with these static fires, we record and evaluate the fire pixel density for each fire object at each time step. When a small fire ( 20 per km2), it is considered to be a static fire and subsequently labelled as invalid.Similar to the retrospective FEDS, we use the active fire detections to create an object serialization product, a regional snapshot GIS product, and a time series product of large fire evolution twice daily. This experimental NRT data will be available upon publication through a university hosted server. More

  • in

    Whales from space dataset, an annotated satellite image dataset of whales for training machine learning models

    Very high-resolution (VHR) satellite imagery allows us to survey regularly remote and large areas of the ocean, difficult to access by boats or planes. The interest in using VHR satellite imagery for the study of great whales (including sperm whales and baleen whales) has grown in the past years1,2,3,4,5 since Abileah6 and Fretwell et al.7 showed its potential. This growing interest may be linked to the improvement in the spatial resolution of satellite imagery, which increased in 2014 from 46 cm to 31 cm. This upgrade enhanced the confidence in the detection of whales in satellite imagery, as more details could be seen, such as whale-defining features (e.g. flukes).Detecting whales in the imagery is either conducted manually1,4,5,7, or automatically2,3. A downside of the manual approach is that it is time-demanding, with manual counter often having to view hundred and sometimes thousands of square kilometres of open ocean. The development of automated approaches to detect whales by satellite would not only speed up this application, but also reduce the possibility of missing whales due to observer fatigue and standardize the procedure. Various automated approaches exist from pixel-based to artificial intelligence. Machine learning, an application of artificial intelligence, seems to be the most appropriate automated method to detect whales efficiently in satellite imagery2,3,8,9.In machine learning an algorithm learns how to identify features by repeatedly testing different search parameters against a training dataset10,11. Concerning whales, the algorithm needs to be trained to detect the wide variety of shapes and colour characterising whales. Shapes and colour will be influenced by the type of species, the environment (e.g. various degree of turbidity), the light conditions, and the behaviours (e.g. foraging, travelling, breaching), as different behaviours will result in different postures. The larger a training dataset is, the more accurate and transferable to other satellite images the algorithm will be. At the time of writing, such a dataset does not exist or is not publicly available.Creating a large enough dataset necessary to train algorithms to detect whales in VHR satellite imagery will require the various research groups analysing VHR satellite imagery to openly share examples of whales and non-whale objects in VHR satellite imagery, which could be facilitated by uploading such data on a central open source repository, similar to the GenBank12 for DNA code or OBIS-Seamap13 for marine wildlife observations. Ideally clipped out image chips of the whale objects would be shared as tiff files, which retains most of the characteristics of the original image. However, all VHR satellites are commercially owned, except for the Cartosat-3 owned by the government of India14, which means it is not possible to publicly share image chips as tiff file. Instead, image chips could be shared in a png or jepg format, which involve loosing some spectral information. If tiff files are required, georeferenced and labelled boxes encompassing the whale objects could also be shared, including information on the satellite imagery to allow anyone to ask the commercial providers for the exact imagery.Here we present a database of whale objects found in VHR satellite imagery. It represents four different species of whales (i.e. southern right whale, Eubalaena australis; grey whale, Eschrichtius robustus; humpback whale, Megaptera novaeangliae; fin whale, Balaenoptera physalus; Fig. 1), which were manually detected in images captured by different satellites (i.e., GeoEye-1, Quickbird-2, WorldView-2, WorldView-3). We created the database by (i) first detecting whale objects manually in satellite imagery, (ii) then we classified whale objects as either “definite”, “probable” or “possible” as in Cubaynes et al.1; and (iii) finally we created georeferenced and labelled points and boxes centered around each whale object, as well as providing image chips in a png format. With this database made publicly available, we aim to initiate the creation of a central database that can be built upon.Fig. 1Database of annotated whales detected in satellite imagery covering different species and areas. Humpback whales were detected in Maui Nui, US (a); grey whales in Laguna San Ignacio, Mexico (b); fin whales in the Pelagos Sanctuary, France, Monaco and Italy (c); southern right whales were observed in three areas, off the Peninsula Valdes, Argentina (d); off Witsand, South Africa (e); and off the Auckland Islands, New Zealand (f). The dot size represents the number of annotated whales per location. Whale silhouettes were sourced from philopic.com (the grey and humpback whales silhouettes are from Chris Luh).Full size image More

  • in

    Shoaling guppies evade predation but have deadlier parasites

    Everard, M., Johnston, P., Santillo, D. & Staddon, C. The role of ecosystems in mitigation and management of Covid-19 and other zoonoses. Environ. Sci. Policy 111, 7–17 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Alizon, S., Hurford, A., Mideo, N. & Van Baalen, M. Virulence evolution and the trade‐off hypothesis: history, current state of affairs and the future. J. Evolut. Biol. 22, 245–259 (2009).CAS 
    Article 

    Google Scholar 
    Cressler, C. E., McLeod, D. V., Rozins, C., Van Den Hoogen, J. & Day, T. The adaptive evolution of virulence: a review of theoretical predictions and empirical tests. Parasitology 143, 915–930 (2016).PubMed 
    Article 

    Google Scholar 
    Acevedo, M. A., Dillemuth, F. P., Flick, A. J., Faldyn, M. J. & Elderd, B. D. Virulence‐driven trade‐offs in disease transmission: a meta‐analysis. Evolution 73, 636–647 (2019).PubMed 
    Article 

    Google Scholar 
    Anderson, R. M. & May, R. M. Coevolution of hosts and parasites. Parasitology 85, 411–426 (1982).PubMed 
    Article 

    Google Scholar 
    McKay, B., Ebell, M., Dale, A. P., Shen, Y. & Handel, A. Virulence-mediated infectiousness and activity trade-offs and their impact on transmission potential of influenza patients. Proc. R. Soc. B 287, 20200496 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bonneaud, C. et al. Experimental evidence for stabilizing selection on virulence in a bacterial pathogen. Evol. Lett. 4, 491–501 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    De Roode, J. C., Yates, A. J. & Altizer, S. Virulence–transmission trade-offs and population divergence in virulence in a naturally occurring butterfly parasite. Proc. Natl Acad. Sci. USA 105, 7489–7494 (2008).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Fraser, C., Hollingsworth, T. D., Chapman, R., de Wolf, F. & Hanage, W. P. Variation in HIV-1 set-point viral load: epidemiological analysis and an evolutionary hypothesis. Proc. Natl Acad. Sci. USA 104, 17441–17446 (2007).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Choo, K., Williams, P. D. & Day, T. Host mortality, predation and the evolution of parasite virulence. Ecol. Lett. 6, 310–315 (2003).Article 

    Google Scholar 
    Williams, P. D. & Day, T. Interactions between sources of mortality and the evolution of parasite virulence. Proc. R. Soc. B 268, 2331–2337 (2001).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Gandon, S., Jansen, V. A. & Van Baalen, M. Host life history and the evolution of parasite virulence. Evolution 55, 1056–1062 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    Prado, F., Sheih, A., West, J. D. & Kerr, B. Coevolutionary cycling of host sociality and pathogen virulence in contact networks. J. Theor. Biol. 261, 561–569 (2009).PubMed 
    Article 

    Google Scholar 
    Herre, E. A. Population structure and the evolution of virulence in nematode parasites of fig wasps. Science 259, 1442–1445 (1993).CAS 
    PubMed 
    Article 

    Google Scholar 
    Boots, M. & Mealor, M. Local interactions select for lower pathogen infectivity. Science 315, 1284–1286 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Alizon, S., de Roode, J. C. & Michalakis, Y. Multiple infections and the evolution of virulence. Ecol. Lett. 16, 556–567 (2013).PubMed 
    Article 

    Google Scholar 
    Bull, J. J. & Lauring, A. S. Theory and empiricism in virulence evolution. PLoS Pathog. 10, e1004387 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Brown, S. P., Hochberg, M. E. & Grenfell, B. T. Does multiple infection select for raised virulence? Trends Microbiol. 10, 401–405 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    Peacor, S. D. & Werner, E. E. The contribution of trait-mediated indirect effects to the net effects of a predator. Proc. Natl Acad. Sci. USA 98, 3904–3908 (2001).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Seppälä, O., Karvonen, A. & Valtonen, E. T. Shoaling behaviour of fish under parasitism and predation risk. Anim. Behav. 75, 145–150 (2008).Article 

    Google Scholar 
    Lopez, L. K. & Duffy, M. A. Mechanisms by which predators mediate host–parasite interactions in aquatic systems. Trends Parasitol. 37, 890–906 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Rigby, M. C. & Jokela, J. Predator avoidance and immune defence: costs and trade-offs in snails. Proc. R. Soc. B 267, 171–176 (2000).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Krause, J., Ruxton, G. D., Ruxton, G. & Ruxton, I. G. Living in Groups (Oxford Univ. Press, 2002).Godin, J.-G. J. Antipredator function of shoaling in teleost fishes: a selective review. Nat. Can. 113, 241–250 (1986).
    Google Scholar 
    Gandon, S., van Baalen, M. & Jansen, V. A. The evolution of parasite virulence, superinfection, and host resistance. Am. Nat. 159, 658–669 (2002).PubMed 
    Article 

    Google Scholar 
    Magurran, A. E. Evolutionary Ecology: The Trinidadian Guppy (Oxford Univ. Press, 2005).Magurran, A. E. & Seghers, B. H. Variation in schooling and aggression amongst guppy (Poecilia reticulata) populations in Trinidad. Behaviour 118, 214–234 (1991).Article 

    Google Scholar 
    Seghers, B. H. & Magurran, A. E. Predator inspection behaviour covaries with schooling tendency amongst wild guppy, Poecilia reticulata, populations in Trinidad. Behaviour 128, 121–134 (1994).Article 

    Google Scholar 
    Huizinga, M., Ghalambor, C. & Reznick, D. The genetic and environmental basis of adaptive differences in shoaling behaviour among populations of Trinidadian guppies, Poecilia reticulata. J. Evolut. Biol. 22, 1860–1866 (2009).CAS 
    Article 

    Google Scholar 
    Stephenson, J. F., Van Oosterhout, C., Mohammed, R. S. & Cable, J. Parasites of Trinidadian guppies: evidence for sex‐ and age‐specific trait‐mediated indirect effects of predators. Ecology 96, 489–498 (2015).PubMed 
    Article 

    Google Scholar 
    Richards, E. L., Van Oosterhout, C. & Cable, J. Sex-specific differences in shoaling affect parasite transmission in guppies. PLoS ONE 5, e13285 (2010).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Johnson, M. B., Lafferty, K. D., Van Oosterhout, C. & Cable, J. Parasite transmission in social interacting hosts: monogenean epidemics in guppies. PLoS ONE https://doi.org/10.1371/journal.pone.0022634 (2011).Gotanda, K. M. et al. Adding parasites to the guppy-predation story: insights from field surveys. Oecologia 172, 155–166 (2013).PubMed 
    Article 

    Google Scholar 
    Fraser, B. A., Ramnarine, I. W. & Neff, B. D. Temporal variation at the MHC class IIB in wild populations of the guppy (Poecilia reticulata). Evolution 64, 2086–2096 (2010).PubMed 

    Google Scholar 
    Stephenson, J. F. et al. Host heterogeneity affects both parasite transmission to and fitness on subsequent hosts. Philos. Trans. R. Soc. B 372, 20160093 (2017).Article 

    Google Scholar 
    Cable, J. & Van Oosterhout, C. The impact of parasites on the life history evolution of guppies (Poecilia reticulata): the effects of host size on parasite virulence. Int. J. Parasitol. 37, 1449–1458 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Reznick, D. N., Butler, M. J. IV, Rodd, F. H. & Ross, P. Life‐history evolution in guppies (Poecilia reticulata) 6. Differential mortality as a mechanism for natural selection. Evolution 50, 1651–1660 (1996).PubMed 

    Google Scholar 
    Bonds, M. H., Keenan, D. C., Leidner, A. J. & Rohani, P. Higher disease prevalence can induce greater sociality: a game theoretic coevolutionary model. Evolution 59, 1859–1866 (2005).PubMed 
    Article 

    Google Scholar 
    Kerr, B., Neuhauser, C., Bohannan, B. J. & Dean, A. M. Local migration promotes competitive restraint in a host–pathogen ‘tragedy of the commons’. Nature 442, 75–78 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    Boots, M. & Sasaki, A. ‘Small worlds’ and the evolution of virulence: infection occurs locally and at a distance. Proc. R. Soc. B 266, 1933–1938 (1999).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Wild, G., Gardner, A. & West, S. A. Adaptation and the evolution of parasite virulence in a connected world. Nature 459, 983–986 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    Dargent, F., Rolshausen, G., Hendry, A., Scott, M. & Fussmann, G. Parting ways: parasite release in nature leads to sex‐specific evolution of defence. J. Evolut. Biol. 29, 23–34 (2016).CAS 
    Article 

    Google Scholar 
    Reznick, D. A., Bryga, H. & Endler, J. A. Experimentally induced life-history evolution in a natural population. Nature 346, 357–359 (1990).Article 

    Google Scholar 
    Stephenson, J. F., van Oosterhout, C. & Cable, J. Pace of life, predators and parasites: predator-induced life-history evolution in Trinidadian guppies predicts decrease in parasite tolerance. Biol. Lett. 11, 20150806 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Stephenson, J. F., Stevens, M., Troscianko, J. & Jokela, J. The size, symmetry, and color saturation of a male guppy’s ornaments forecast his resistance to parasites. Am. Naturalist 196, 597–608 (2020).Article 

    Google Scholar 
    Godin, J.-G. J. & McDonough, H. E. Predator preference for brightly colored males in the guppy: a viability cost for a sexually selected trait. Behav. Ecol. 14, 194–200 (2003).Article 

    Google Scholar 
    Van Oosterhout, C., Harris, P. & Cable, J. Marked variation in parasite resistance between two wild populations of the Trinidadian guppy, Poecilia reticulata (Pisces: Poeciliidae). Biol. J. Linn. Soc. 79, 645–651 (2003).Article 

    Google Scholar 
    Hawley, D. M., Gibson, A. K., Townsend, A. K., Craft, M. E. & Stephenson, J. F. Bidirectional interactions between host social behaviour and parasites arise through ecological and evolutionary processes. Parasitology 148, 274–288 (2020).PubMed 
    Article 

    Google Scholar 
    Janecka, M. J., Rovenolt, F. & Stephenson, J. F. How does host social behavior drive parasite non-selective evolution from the within-host to the landscape-scale? Behav. Ecol. Sociobiol. 75, 1–20 (2021).Article 

    Google Scholar 
    Tao, H., Li, L., White, M. C., Steel, J. & Lowen, A. C. Influenza A virus coinfection through transmission can support high levels of reassortment. J. Virol. 89, 8453–8461 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Eshel, I. Evolutionary and continuous stability. J. Theor. Biol. 103, 99–111 (1983).Article 

    Google Scholar 
    Hurford, A., Cownden, D. & Day, T. Next-generation tools for evolutionary invasion analyses. J. R. Soc. Interface 7, 561–571 (2009).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Leimar, O. Multidimensional convergence stability. Evolut. Ecol. Res. 11, 191–208 (2009).
    Google Scholar 
    Reznick, D., Bryant, M. & Holmes, D. The evolution of senescence and post-reproductive lifespan in guppies (Poecilia reticulata). PLoS Biol. 4, e7 (2005).PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Stephenson, J. F. Parasite-induced plasticity in host social behaviour depends on sex and susceptibility. Biol. Lett. https://doi.org/10.1098/rsbl.2019.0557 (2019).Lopez, S. Acquired resistance affects male sexual display and female choice in guppies. Proc. R. Soc. B 265, 717–723 (1998).Article 

    Google Scholar 
    van Oosterhout, C. et al. Selection by parasites in spate conditions in wild Trinidadian guppies (Poecilia reticulata). Int. J. Parasitol. 37, 805–812 (2007).PubMed 
    Article 

    Google Scholar 
    Pérez-Jvostov, F., Hendry, A. P., Fussmann, G. F. & Scott, M. E. Are host–parasite interactions influenced by adaptation to predators? A test with guppies and Gyrodactylus in experimental stream channels. Oecologia 170, 77–88 (2012).PubMed 
    Article 

    Google Scholar 
    Eiben, A. E. & Smith, J. E. Introduction to Evolutionary Computing (Springer, 2003).Carnell, R. lhs: Latin hypercube samples v.1.1.1 (R-Project, 2020).Iooss, B., Da Veiga, S., Janon, A. & Pujol, G. Sensitivity: Global sensitivity analysis of model outputs v.1.25.0 (R-Project, 2021).Wright, D. & Krause, J. Repeated measures of shoaling tendency in zebrafish (Danio rerio) and other small teleost fishes. Nat. Protoc. 1, 1828–1831 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    Friard, O. & Gamba, M. BORIS: a free, versatile open‐source event‐logging software for video/audio coding and live observations. Methods Ecol. Evol. 7, 1325–1330 (2016).Article 

    Google Scholar 
    Griffiths, S. W. & Magurran, A. E. Sex and schooling behaviour in the Trinidadian guppy. Anim. Behav. 56, 689–693 (1998).CAS 
    PubMed 
    Article 

    Google Scholar 
    Magurran, A., Seghers, B., Carvalho, G. & Shaw, P. Behavioural consequences of an artificial introduction of guppies (Poecilia reticulata) in N. Trinidad: evidence for the evolution of anti-predator behaviour in the wild. Proc. R. Soc. B 248, 117–122 (1992).Article 

    Google Scholar 
    Sievers, C. et al. Reasons for the invasive success of a guppy (Poecilia reticulata) population in Trinidad. PLoS ONE 7, e38404 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Mohammed, R. S. et al. Parasite diversity and ecology in a model species, the guppy (Poecilia reticulata) in Trinidad. R. Soc. Open Sci. 7, 191112 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lyles, A. M. Genetic Variation and Susceptibility to Parasites: Poeclia reticulata Infected with Gyrodactylus turnbulli. PhD dissertation, Princeton Univ. (1990).Fraser, B. A. & Neff, B. D. Parasite mediated homogenizing selection at the MHC in guppies. Genetica 138, 273 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    Reznick, D. & Endler, J. A. The impact of predation on life history evolution in Trinidadian guppies (Poecilia reticulata). Evolution 36, 160–177 (1982).PubMed 

    Google Scholar 
    El‐Sabaawi, R. W. et al. Assessing the effects of guppy life history evolution on nutrient recycling: from experiments to the field. Freshw. Biol. 60, 590–601 (2015).Article 

    Google Scholar 
    Liley, N. & Luyten, P. Geographic variation in the sexual behaviour of the guppy, Poecilia reticulata (Peters). Behaviour 95, 164–179 (1985).Article 

    Google Scholar 
    Reznick, D. N. et al. Eco-evolutionary feedbacks predict the time course of rapid life-history evolution. Am. Nat. 194, 671–692 (2019).PubMed 
    Article 

    Google Scholar  More

  • in

    A trait database and updated checklist for European subterranean spiders

    Zanne, A. E. et al. Fungal functional ecology: bringing a trait-based approach to plant-associated fungi. Biol. Rev. 95, 409–433 (2020).PubMed 
    Article 

    Google Scholar 
    Põlme, S. et al. FungalTraits: a user-friendly traits database of fungi and fungus-like stramenopiles. Fungal Divers. 105, 1–16 (2020).Article 

    Google Scholar 
    Fraser, L. H. TRY—A plant trait database of databases. Glob. Chang. Biol. 26, 189–190 (2020).ADS 
    PubMed 
    Article 

    Google Scholar 
    Kattge, J. et al. TRY plant trait database – enhanced coverage and open access. Glob. Chang. Biol. 26, 119–188 (2020).ADS 
    PubMed 
    Article 

    Google Scholar 
    Oliveira, B. F., São-Pedro, V. A., Santos-Barrera, G., Penone, C. & Costa, G. C. AmphiBIO, a global database for amphibian ecological traits. Sci. Data 4, 170123 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lecocq, T. et al. TOFF, a database of traits of fish to promote advances in fish aquaculture. Sci. Data 6, 301 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Jones, K. E. et al. PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals. Ecology 90, 2648 (2009).Article 

    Google Scholar 
    Parr, C. L. et al. GlobalAnts: a new database on the geography of ant traits (Hymenoptera: Formicidae). Insect Conserv. Divers. 10, 5–20 (2017).Article 

    Google Scholar 
    Homburg, K., Homburg, N., Schäfer, F., Schuldt, A. & Assmann, T. Carabids.org – a dynamic online database of ground beetle species traits (Coleoptera, Carabidae). Insect Conserv. Divers. 7, 195–205 (2014).Article 

    Google Scholar 
    Lowe, E. C. et al. Towards establishment of a centralized spider traits database. J. Arachnol. 48 (2020).Tobias, J. A. et al. AVONET: morphological, ecological and geographical data for all birds. Ecol. Lett. 25, 581–597 (2022).PubMed 
    Article 

    Google Scholar 
    Mammola, S., Carmona, C. P., Guillerme, T. & Cardoso, P. Concepts and applications in functional diversity. Funct. Ecol. 35, 1869–1885 (2021).Article 

    Google Scholar 
    de Bello, F. et al. Handbook of trait-based ecology: from theory to R tools. (Cambridge University Press, 2021).Edwards, K. F. et al. Evolutionarily stable communities: a framework for understanding the role of trait evolution in the maintenance of diversity. Ecol. Lett. 21, 1853–1868 (2018).PubMed 
    Article 

    Google Scholar 
    McGill, B. J., Enquist, B. J., Weiher, E. & Westoby, M. Rebuilding community ecology from functional traits. Trends Ecol. Evol. 21, 178–185 (2006).PubMed 
    Article 

    Google Scholar 
    Violle, C., Reich, P. B., Pacala, S. W., Enquist, B. J. & Kattge, J. The emergence and promise of functional biogeography. Proc. Natl. Acad. Sci. 111, 13690–13696 (2014).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kosman, E., Burgio, K. R., Presley, S. J., Willig, M. R. & Scheiner, S. M. Conservation prioritization based on trait‐based metrics illustrated with global parrot distributions. Divers. Distrib. 25, 1156–1165 (2019).Article 

    Google Scholar 
    Cadotte, M. W., Carscadden, K. & Mirotchnick, N. Beyond species: functional diversity and the maintenance of ecological processes and services. J. Appl. Ecol. 48, 1079–1087 (2011).Article 

    Google Scholar 
    de Bello, F. et al. Towards an assessment of multiple ecosystem processes and services via functional traits. Biodivers. Conserv. 19, 2873–2893 (2010).Article 

    Google Scholar 
    Ficetola, G. F., Canedoli, C. & Stoch, F. The Racovitzan impediment and the hidden biodiversity of unexplored environments. Conserv. Biol. 33, 214–216 (2019).PubMed 
    Article 

    Google Scholar 
    Mammola, S. et al. Collecting eco-evolutionary data in the dark: Impediments to subterranean research and how to overcome them. Ecol. Evol. 11, 5911–5926 (2021).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Mammola, S. et al. Fundamental research questions in subterranean biology. Biol. Rev. 95, 1855–1872 (2020).PubMed 
    Article 

    Google Scholar 
    Cardoso, P. Diversity and community assembly patterns of epigean vs. troglobiont spiders in the Iberian Peninsula. Int. J. Speleol. 41, 83–94 (2012).Article 

    Google Scholar 
    Fernandes, C. S., Batalha, M. A. & Bichuette, M. E. Does the cave environment reduce functional diversity? PLoS One 11, e0151958 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Saccò, M. et al. New light in the dark – a proposed multidisciplinary framework for studying functional ecology of groundwater fauna. Sci. Total Environ. 662, 963–977 (2019).ADS 
    PubMed 
    Article 
    CAS 

    Google Scholar 
    Mammola, S. & Isaia, M. Spiders in caves. Proceedings of the Royal Society B: Biological Sciences 284, 20170193 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Parimuchová, A. et al. The food web in a subterranean ecosystem is driven by intraguild predation. Sci. Rep. 11, 4994 (2021).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Bloom, T. et al. Discovery of two new species of eyeless spiders within a single Hispaniola cave. J. Arachnol. 42, 148–154 (2014).Article 

    Google Scholar 
    Mammola, S., Cardoso, P., Ribera, C., Pavlek, M. & Isaia, M. A synthesis on cave-dwelling spiders in Europe. J. Zool. Syst. Evol. Res. 56, 301–316 (2018).Article 

    Google Scholar 
    Mammola, S. et al. Continental data on cave-dwelling spider communities across Europe (Arachnida: Araneae). Biodivers. Data J. 7, e38492 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Milano, F. et al. Spider conservation in Europe: a review. Biol. Conserv. 256, 109020 (2021).Article 

    Google Scholar 
    Pekár, S. et al. The World Spider Trait database (WST): a centralised global open repository for curated data on spider traits. Database 2021, baab064 (2021).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ledesma, E., Jiménez-Valverde, A., de Castro, A., Aguado-Aranda, P. & Ortuño, V. M. The study of hidden habitats sheds light on poorly known taxa: spiders of the Mesovoid Shallow Substratum. Zookeys 841, 39–59 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    World Spider Catalog. World Spider Catalog. Version 23.0. Natural History Museum Bern 10.24436/2 (2022).Nentwig, W. et al. Araneae – Spider of Europe. 10.24436/1 (2021).Malumbres-Olarte, J. et al. Habitat filtering and inferred dispersal ability condition across-scale species turnover and rarity in Macaronesian island spider assemblages. J. Biogeogr. 48, 3131–3144 (2021).Article 

    Google Scholar 
    Nentwig, W., Gloor, D. & Kropf, C. Spider taxonomists catch data on web. Nature 528, 479 (2015).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Mammola, S. et al. Environmental filtering and convergent evolution determine the ecological specialization of subterranean spiders. Funct. Ecol. 34, 1064–1077 (2020).Article 

    Google Scholar 
    Mammola, S. et al. Ecological speciation in darkness? Spatial niche partitioning in sibling subterranean spiders (Araneae: Linyphiidae: Troglohyphantes). Invertebr. Syst. 32, 1069–1082 (2018).Article 

    Google Scholar 
    Huber, B. A. Cave-dwelling pholcid spiders (Araneae, Pholcidae): A review. Subterr. Biol. 26, 1–18 (2018).ADS 
    Article 

    Google Scholar 
    Arnedo, M. A., Oromí, P., Múrria, C., Macías-Hernández, N. & Ribera, C. The dark side of an island radiation: systematics and evolution of troglobitic spiders of the genus Dysdera Latreille (Araneae:Dysderidae) in the Canary Islands. Invertebr. Syst. 21, 623–660 (2007).Article 

    Google Scholar 
    Ubick, D., Paquin, P., Cushing, P. E. & Duperre, N. Spiders of North America: An Identification Manual. (Amer Arachnological Society, 2007).Cardoso, P., Pekár, S., Jocqué, R. & Coddington, J. A. Global patterns of guild composition and functional diversity of spiders. PLoS One 6, e21710 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Smithers, P. The early life history and dispersal of the cave spider Meta menardi (Latreille, 1804) (Araneae: Tetragnathidae). Bull. Br. arachnol. Soc 13, 213–216 (2005).
    Google Scholar 
    Mammola, S., Hormiga, G., Arnedo, M. A. & Isaia, M. Unexpected diversity in the relictual European spiders of the genus Pimoa (Araneae:Pimoidae). Invertebr. Syst. 30, 566–587 (2016).Article 

    Google Scholar 
    Sket, B. Can we agree on an ecological classification of subterranean animals? J. Nat. Hist. 42, 1549–1563 (2008).Article 

    Google Scholar 
    Trajano, E. & de Carvalho, M. R. Towards a biologically meaningful classification of subterranean organisms: A critical analysis of the schiner-racovitza system from a historical perspective, difficulties of its application and implications for conservation. Subterr. Biol. 22, 1–26 (2017).Article 

    Google Scholar 
    Martínez, A. & Mammola, S. Specialized terminology reduces the number of citations to scientific papers. Proc. R. Soc. B Biol. Sci. 288, 20202581 (2021).Article 

    Google Scholar 
    Mammola, S. Finding answers in the dark: caves as models in ecology fifty years after Poulson and White. Ecography 42, 1331–1351 (2019).Article 

    Google Scholar 
    Mammola, S. et al. Quantifying troglomorphism in hyperspace. Arpha Conf. Abstr. 5, e82941 (2022).Wickham, H. ggplot2: Elegant Graphics for Data Analysis. (Springer-Verlag, 2016).Palacio, F. X. et al. A protocol for reproducible functional diversity analyses. EcoEvoRxiv https://doi.org/10.32942/osf.io/yt9sb (2022).Article 

    Google Scholar 
    Gower, J. C. A General Coefficient of Similarity and Some of Its Properties. Biometrics 27, 857–871 (1971).Article 

    Google Scholar 
    de Bello, F., Botta-Dukát, Z., Lepš, J. & Fibich, P. Towards a more balanced combination of multiple traits when computing functional differences between species. Methods Ecol. Evol. 12, 443–448 (2021).Article 

    Google Scholar 
    Paradis, E. & Schliep, K. Ape 5.0: An environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Oksanen, J. et al. R Package vegan: community ecology package. R package version 2.5-3 (2018).R Core Team. R: A language and environment for statistical computing. (2021).Mammola, S. A trait database for European subterranean spiders, Figshare, https://doi.org/10.6084/m9.figshare.16574255 (2022).Cardoso, P. & Pekar, S. arakno – An R package for effective spider nomenclature, distribution, and trait data retrieval from online resources. J. Arachnol. 50, 30–32 (2022).Article 

    Google Scholar 
    Johnson, T. F., Isaac, N. J. B., Paviolo, A. & González-Suárez, M. Handling missing values in trait data. Glob. Ecol. Biogeogr. 30, 51–62 (2021).Article 

    Google Scholar 
    Podani, J., Kalapos, T., Barta, B. & Schmera, D. Principal component analysis of incomplete data – A simple solution to an old problem. Ecol. Inform. 61, 101235 (2021).Article 

    Google Scholar 
    Cardoso, P., Mammola, S., Rigal, F. & Carvalho, J. C. BAT: Biodiversity Assessment Tools. R package version 2.6.0 (2021).Cardoso, P., Rigal, F. & Carvalho, J. C. BAT – Biodiversity Assessment Tools, an R package for the measurement and estimation of alpha and beta taxon, phylogenetic and functional diversity. Methods Ecol. Evol. 6, 232–236 (2015).Article 

    Google Scholar 
    De Bello, F. et al. Quantifying the relevance of intraspecific trait variability for functional diversity. Methods Ecol. Evol. 2, 163–174 (2011).Article 

    Google Scholar 
    Violle, C. et al. The return of the variance: intraspecific variability in community ecology. Trends Ecol. Evol. 27, 244–252 (2012).PubMed 
    Article 

    Google Scholar 
    Gentile, G., Bonelli, S. & Riva, F. Evaluating intraspecific variation in insect trait analysis. Ecol. Entomol. 46, 11–18 (2020).Article 

    Google Scholar 
    Wong, M. K. L. & Carmona, C. P. Including intraspecific trait variability to avoid distortion of functional diversity and ecological inference: Lessons from natural assemblages. Methods Ecol. Evol. 12, 946–957 (2021).Article 

    Google Scholar 
    Mammola, S., Piano, E., Malard, F., Vernon, P. & Isaia, M. Extending Janzen’s hypothesis to temperate regions: a test using subterranean ecosystems. Funct. Ecol. 33, 1638–1650 (2019).Article 

    Google Scholar 
    Kratochvíl, J. Araignées cavernicoles des îles Dalmates. Přírodovědné práce ústavů Československé Akad. Věd v Brně 12, 1–59 (1978).
    Google Scholar 
    Denny, M. The fallacy of the average: on the ubiquity, utility and continuing novelty of Jensen’s inequality. J. Exp. Biol. 220, 139–146 (2017).PubMed 
    Article 

    Google Scholar 
    Mammola, S. et al. Cave_dwelling_spiders_Europe. Figshare https://doi.org/10.6084/m9.figshare.8224025.v1 (2019).Darwin, C. On the origin of species by means of natural selection, or the preservation of favoured races in the struggle of life. (John Murray, 1859).Wong, M. K. L., Guénard, B. & Lewis, O. T. Trait-based ecology of terrestrial arthropods. Biol. Rev. 94, 999–1022 (2019).PubMed 
    Article 

    Google Scholar 
    Lučić, I. Interview with Boris Sket: nothing has a sense in speleobiology, without a comparison of cave animals with the ‘normal’ epigean ones. Acta Carsologica 50, 5–9 (2021).Article 

    Google Scholar 
    McGill, B. J. The what, how and why of doing macroecology. Glob. Ecol. Biogeogr. 28, 6–17 (2019).Article 

    Google Scholar 
    Muscarella, R. & Uriarte, M. Do community-weighted mean functional traits reflect optimal strategies? Proc. R. Soc. B Biol. Sci. 283, 20152434 (2016).Article 

    Google Scholar 
    Petchey, O. L. & Gaston, K. J. Functional diversity (FD), species richness and community composition. Ecol. Lett. 5, 402–411 (2002).Article 

    Google Scholar 
    Mammola, S. & Cardoso, P. Functional diversity metrics using kernel density n-dimensional hypervolumes. Methods Ecol. Evol. 11, 986–995 (2020).Article 

    Google Scholar 
    Mammola, S. et al. Local- versus broad-scale environmental drivers of continental β-diversity patterns in subterranean spider communities across Europe. Proc. R. Soc. B Biol. Sci. 286, 20191579 (2019).Article 

    Google Scholar 
    Graco-Roza, C. et al. Distance decay 2.0 – a global synthesis of taxonomic and functional turnover in ecological communities. Glob. Ecol. Biogeogr, in press (available at https://doi.org/10.1101/2021.03.17.435827) (2022).Gallagher, R. V. et al. A guide to using species trait data in conservation. One Earth 4, 927–936 (2021).ADS 
    Article 

    Google Scholar 
    Chichorro, F., Juslén, A. & Cardoso, P. A review of the relation between species traits and extinction risk. Biol. Conserv. 237, 220–229 (2019).Article 

    Google Scholar 
    Chichorro, F. et al. Species traits predict extinction risk across the Tree of Life. bioRxiv 2020.07.01.183053 (2020).Violle, C. et al. Functional rarity: the ecology of outliers. Trends Ecol. Evol. 32, 356–367 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Carmona, C. P. et al. Erosion of global functional diversity across the tree of life. Sci. Adv. 7, eabf2675 (2021).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Loreau, M. et al. Biodiversity as insurance: from concept to measurement and application. Biol. Rev. 96, 2333–2354 (2021).PubMed 
    Article 

    Google Scholar 
    Sánchez-Fernández, D., Galassi, D. M. P., Wynne, J. J., Cardoso, P. & Mammola, S. Don’t forget subterranean ecosystems in climate change agendas. Nat. Clim. Chang. 11, 458–459 (2021).ADS 
    Article 

    Google Scholar 
    Borges, P. A. V. et al. Volcanic caves: Priorities for conserving the Azorean endemic troglobiont species. Int. J. Speleol. 41, 101–112 (2012).Article 

    Google Scholar 
    Rabelo, L. M., Souza-Silva, M. & Ferreira, R. L. Priority caves for biodiversity conservation in a key karst area of Brazil: comparing the applicability of cave conservation indices. Biodivers. Conserv. 27, 2097–2129 (2018).Article 

    Google Scholar 
    Nitzu, E. et al. Assessing preservation priorities of caves and karst areas using the frequency of endemic cave-dwelling species. Int. J. Speleol. 47, 43–52 (2018).Article 

    Google Scholar 
    Pipan, T., Deharveng, L. & Culver, D. C. Hotspots of subterranean biodiversity. Diversity 12, 209 (2020).Article 

    Google Scholar 
    Fattorini, S., Fiasca, B., Di Lorenzo, T., Di Cicco, M. & Galassi, D. M. P. A new protocol for assessing the conservation priority of groundwater-dependent ecosystems. Aquat. Conserv. Mar. Freshw. Ecosyst. 30, 1483–1504 (2020).Article 

    Google Scholar 
    Iannella, M. et al. Getting the ‘most out of the hotspot’ for practical conservation of groundwater biodiversity. Glob. Ecol. Conserv. e01844 (2021).Mazel, F. et al. Prioritizing phylogenetic diversity captures functional diversity unreliably. Nat. Commun. 9, 2888 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Cadotte, M. W. & Tucker, C. M. Difficult decisions: Strategies for conservation prioritization when taxonomic, phylogenetic and functional diversity are not spatially congruent. Biol. Conserv. 225, 128–133 (2018).Article 

    Google Scholar 
    Hanson, J. O. et al. Global conservation of species’ niches. Nature 580, 232–234 (2020).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Pollock, L. J. et al. Protecting biodiversity (in all its complexity): new models and methods. Trends Ecol. Evol. 35, 1119–1128 (2020).PubMed 
    Article 

    Google Scholar 
    Mammola, S. et al. Scientists’ warning on the conservation of subterranean ecosystems. Bioscience 69, 641–650 (2019).Article 

    Google Scholar 
    Wynne, J. J. et al. A conservation roadmap for the subterranean biome. Conserv. Lett. 14, e12834 (2021).Article 

    Google Scholar 
    Mammola, S. et al. Towards evidence-based conservation of subterranean ecosystems. Biol. Rev., early view at https://doi.org/10.1111/brv.12851 (2022).Culver, D. C. & Pipan, T. The biology of caves and other subterranean habitats. (Oxford University Press, USA, 2014).Culver, D. C. & Pipan, T. Shallow Subterranean Habitats: Ecology, Evolution, and Convervation. (Oxford University Press, USA, 2014).Sobral, M. All traits are functional: an evolutionary viewpoint. Trends Plant Sci. 26, 674–676 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Pipan, T. & Culver, D. C. The unity and diversity of the subterranean realm with respect to invertebrate body size. J. Cave Karst Stud. 79, 1–9 (2017).Article 

    Google Scholar 
    Elgar, M. A., Ghaffar, N. & Read, A. F. Sexual dimorphism in leg length among orb-weaving spiders: a possible role for sexual cannibalism. J. Zool. 222, 455–470 (1990).Article 

    Google Scholar 
    Deeleman-Reinhold, C. L. Revision of the cave-dwelling and related spiders of the genus Troglohyphantes Joseph (Linyphiidae), with special reference to the Yugoslav species. Opera Acad. Sci. Artium Slov. 23 (1978).Isaia, M. & Pantini, P. New data on the spider genus Troglohyphantes (Araneae, Linyphiidae) in the Italian Alps, with the description of a new species and a new synonymy. Zootaxa 2690, 1–18 (2010).Article 

    Google Scholar 
    Hagstrum, D. W. Carapace width as a tool for evaluating the rate of development of spiders in the laboratory and the field. Ann. Entomol. Soc. Am. 64, 757–760 (1971).Article 

    Google Scholar 
    Pavlek, M. & Mammola, S. Niche-based processes explaining the distributions of closely related subterranean spiders. J. Biogeogr. 48, 118–133 (2020).Article 

    Google Scholar 
    Mammola, S. Modelling the future spread of native and alien congeneric species in subterranean habitats – The case of meta cave-dwelling spiders in Great Britain. Int. J. Speleol. 46, 427–437 (2017).Article 

    Google Scholar 
    Novak, T. et al. Niche partitioning in orbweaving spiders Meta menardi and Metellina merianae (Tetragnathidae). Acta Oecologica 36, 522–529 (2010).ADS 
    Article 

    Google Scholar 
    Lunghi, E. Occurrence of the Black lace-weaver spider, Amaurobius ferox, in caves. Acta Carsologica 49, 119–124 (2020).Article 

    Google Scholar 
    Isaia, M. & Chiarle, A. Taxonomic notes on Cybaeus vignai Brignoli, 1977 (Araneae, Cybaeidae) and Dysdera cribrata Simon, 1882 (Araneae, Dysderidae) from the Italian Maritime Alps. Zoosystema 37, 45–56 (2015).Article 

    Google Scholar 
    Ledford, J. et al. Phylogenomics and biogeography of leptonetid spiders (Araneae: Leptonetidae). Invertebr. Syst. 35, 332–349 (2021).
    Google Scholar 
    Isaia, M., Mammola, S., Mazzuca, P., Arnedo, M. A. & Pantini, P. Advances in the systematics of the spider genus Troglohyphantes (Araneae, Linyphiidae). Syst. Biodivers. 15, 307–326 (2017).Article 

    Google Scholar 
    Hajer, J. & Řeháková, D. Spinning activity of the spider Trogloneta granulum (Araneae, Mysmenidae): web, cocoon, cocoon handling behaviour, draglines and attachment discs. Zoology 106, 223–231 (2003).PubMed 
    Article 

    Google Scholar 
    Huber, B. A., Pavlek, M. & Komnenov, M. Revision of the spider genus Stygopholcus (Araneae, Pholcidae), endemic to the Balkan Peninsula. Eur. J. Taxon. 752, 1–60 (2021).
    Google Scholar 
    Huber, B. A. Revision of the spider genus Hoplopholcus Kulczyński (Araneae, Pholcidae). Zootaxa 4726, 1–94 (2020).Article 

    Google Scholar 
    Cardoso, P. & Scharff, N. First record of the spider family symphytognathidae in Europe and description of Anapistula ataecina sp. n. (araneae). Zootaxa 2246, 45–57 (2009).Article 

    Google Scholar 
    Wang, C., Ribera, C. & Li, S. On the identity of the type species of the genus Telema (Araneae, Telemidae). Zookeys 251, 11–19 (2012).Article 

    Google Scholar 
    Hesselberg, T., Simonsen, D. & Juan, C. Do cave orb spiders show unique behavioural adaptations to subterranean life? A review of the evidence. Behaviour 1–28 (2019). More

  • in

    Increased abundance of a common scavenger affects allocation of carrion but not efficiency of carcass removal in the Fukushima Exclusion Zone

    Lim, N., Kelt, D. A., Lim, K. K. & Bernard, H. Vertebrate scavengers control abundance of diarrheal-causing bacteria in tropical plantations. Zool. Stud. 59, 1–10 (2020).
    Google Scholar 
    Beasley, J. C., Olson, Z. H. & DeVault, T. L. Ecological role of vertebrate scavengers. In: Carrion Ecology, Evolution and their Applications. (eds Benbow, E.M., Tomberlin, J. & Tarone, A.) 107–127 (CRC Press, 2015).
    Ogada, D. L., Keesing, F. & Virani, M. Z. Dropping dead: Causes and consequences of vulture population declines worldwide. Ann. N. Y. Acad. Sci. 1249, 57–71 (2012).ADS 
    PubMed 
    Article 

    Google Scholar 
    Reid, W. V. et al. Ecosystems and Human Well-Being-Synthesis: A Report of the Millennium Ecosystem Assessment (Island Press, 2005).
    Google Scholar 
    Wilson, E. E. & Wolkovich, E. M. Scavenging: How carnivores and carrion structure communities. Trends Ecol. Evol. 26, 129–135 (2011).PubMed 
    Article 

    Google Scholar 
    Moleón, M., Sánchez-Zapata, J. A., Selva, N., Donázar, J. A. & Owen-Smith, N. Inter-specific interactions linking predation and scavenging in terrestrial vertebrate assemblages. Biol. Rev. 89, 1042–1054. https://doi.org/10.1111/brv.12097 (2014).Article 
    PubMed 

    Google Scholar 
    Fonseca, C. R. & Ganade, G. Species functional redundancy, random extinctions and the stability of ecosystems. J. Ecol. 89, 118–125 (2001).Article 

    Google Scholar 
    Mori, A. S., Furukawa, T. & Sasaki, T. Response diversity determines the resilience of ecosystems to environmental change. Biol. Rev. 88, 349–364. https://doi.org/10.1111/brv.12004 (2013).Article 
    PubMed 

    Google Scholar 
    Huijbers, C. M. et al. Limited functional redundancy in vertebrate scavenger guilds fails to compensate for the loss of raptors from urbanized sandy beaches. Divers. Distrib. 21, 55–63 (2015).Article 

    Google Scholar 
    Ceballos, G. et al. Accelerated modern human–induced species losses: Entering the sixth mass extinction. Sci. Adv. 1, e1400253 (2015).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Buechley, E. R. & Şekercioğlu, Ç. H. The Avian scavenger crisis: Looming extinctions, trophic cascades, and loss of critical ecosystem functions. Biol. Cons. 198, 220–228 (2016).Article 

    Google Scholar 
    Hill, J. E., DeVault, T. L., Wang, G. & Belant, J. L. Anthropogenic mortality in mammals increases with the human footprint. Front. Ecol. Environ. 18, 13–18. https://doi.org/10.1002/fee.2127 (2019).Article 

    Google Scholar 
    Sebastián-González, E. et al. Scavenging in the Anthropocene: Human impact drives vertebrate scavenger species richness at a global scale. Glob. Change Biol. 25, 3005–3017 (2019).ADS 
    Article 

    Google Scholar 
    Sebastián-González, E. et al. Network structure of vertebrate scavenger assemblages at the global scale: Drivers and ecosystem functioning implications. Ecography 43, 1–13. https://doi.org/10.1111/ecog.05083 (2020).Article 

    Google Scholar 
    Marneweck, C. J., Katzner, T. E. & Jachowski, D. S. Predicted climate-induced reductions in scavenging in eastern North America. Glob. Change Biol. 27, 3383–3394. https://doi.org/10.1111/gcb.15653 (2021).Article 

    Google Scholar 
    Mokany, K., Ash, J. & Roxburgh, S. Functional identity is more important than diversity in influencing ecosystem processes in a temperate native grassland. J. Ecol. 96, 884–893. https://doi.org/10.1111/j.1365-2745.2008.01395.x (2008).Article 

    Google Scholar 
    Gagic, V. et al. Functional identity and diversity of animals predict ecosystem functioning better than species-based indices. Proc. R. Soc. B Biol. Sci. 282, 20142620 (2015).Article 

    Google Scholar 
    Mateo-Tomás, P., Olea, P. P., Selva, N. & Sánchez-Zapata, J. A. Species and individual replacements contribute more than nestedness to shape vertebrate scavenger metacommunities. Ecography 42, 365–375 (2019).Article 

    Google Scholar 
    Sebastián-González, E. et al. Functional traits driving species role in the structure of terrestrial vertebrate scavenger networks. Ecology https://doi.org/10.1002/ecy.3519 (2021).Article 
    PubMed 

    Google Scholar 
    DeVault, T. L., Rhodes, O. E. Jr. & Shivik, J. A. Scavenging by vertebrates: Behavioral, ecological, and evolutionary perspectives on an important energy transfer pathway in terrestrial ecosystems. Oikos 102, 225–234 (2003).Article 

    Google Scholar 
    Allen, M. L., Elbroch, L. M., Wilmers, C. C. & Wittmer, H. U. The comparative effects of large carnivores on the acquisition of carrion by scavengers. Am. Nat. 185, 822–833 (2015).PubMed 
    Article 

    Google Scholar 
    Moleón, M., Sánchez-Zapata, J. A., Sebastián-González, E. & Owen-Smith, N. Carcass size shapes the structure and functioning of an African scavenging assemblage. Oikos 124, 1391–1403 (2015).Article 

    Google Scholar 
    Gutiérrez-Cánovas, C. et al. Large home range scavengers support higher rates of carcass removal. Funct. Ecol. 34, 1921–1932 (2020).Article 

    Google Scholar 
    Walker, M. A. et al. Factors influencing scavenger guilds and scavenging efficiency in Southwestern Montana. Sci. Rep. https://doi.org/10.1038/s41598-021-83426-3 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Winfree, R., Fox, J., Williams, N. M., Reilly, J. R. & Cariveau, D. P. Abundance of common species, not species richness, drives delivery of a real-world ecosystem service. Ecol. Lett. 18, 626–635. https://doi.org/10.1111/ele.12424 (2015).Article 
    PubMed 

    Google Scholar 
    Mateo-Tomás, P., Olea, P. P., Moleón, M., Selva, N. & Sánchez-Zapata, J. A. Both rare and common species support ecosystem services in scavenger communities. Glob. Ecol. Biogeogr. 26, 1459–1470. https://doi.org/10.1111/geb.12673 (2017).Article 

    Google Scholar 
    Butler, J. R. A. & du Toit, J. T. Diet of free-ranging domestic dogs (Canis familiaris) in rural Zimbabwe: Implications for wild scavengers on the periphery of wildlife reserves. Anim. Conserv. 5, 29–37. https://doi.org/10.1017/s136794300200104x (2002).Article 

    Google Scholar 
    DeVault, T. L., Olson, Z. H., Beasley, J. C. & Rhodes, O. E. Jr. Mesopredators dominate competition for carrion in an agricultural landscape. Basic Appl. Ecol. 12, 268–274 (2011).Article 

    Google Scholar 
    Ogada, D. L., Torchin, M. E., Kinnaird, M. F. & Ezenwa, V. O. Effects of vulture declines on facultative scavengers and potential implications for mammalian disease transmission. Conserv. Biol. 26, 453–460. https://doi.org/10.1111/j.1523-1739.2012.01827.x (2012).CAS 
    Article 
    PubMed 

    Google Scholar 
    Morales-Reyes, Z. et al. Scavenging efficiency and red fox abundance in Mediterranean mountains with and without vultures. Acta Oecol. 79, 81–88. https://doi.org/10.1016/j.actao.2016.12.012 (2017).ADS 
    Article 

    Google Scholar 
    Inagaki, A. et al. Vertebrate scavenger guild composition and utilization of carrion in an East Asian temperate forest. Ecol. Evol. 10, 1223–1232 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Blazquez, M., Sanchez-Zapata, J. A., Botella, F., Carrete, M. & Eguía, S. Spatio-temporal segregation of facultative avian scavengers at ungulate carcasses. Acta Oecol. 35, 645–650 (2009).ADS 
    Article 

    Google Scholar 
    Inger, R., Cox, D. T. C., Per, E., Norton, B. A. & Gaston, K. J. Ecological role of vertebrate scavengers in urban ecosystems in the UK. Ecol. Evol. 6, 7015–7023. https://doi.org/10.1002/ece3.2414 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Hill, J. E., DeVault, T. L., Beasley, J. C., Rhodes, O. E. Jr. & Belant, J. L. Effects of vulture exclusion on carrion consumption by facultative scavengers. Ecol. Evol. 8, 2518–2526. https://doi.org/10.1002/ece3.3840 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Olson, Z., Beasley, J., DeVault, T. L. & Rhodes, O. E. Jr. Scavenger community response to the removal of a dominant scavenger. Oikos 121, 77–84 (2012).Article 

    Google Scholar 
    Pardo-Barquín, E., Mateo-Tomás, P. & Olea, P. P. Habitat characteristics from local to landscape scales combine to shape vertebrate scavenging communities. Basic Appl. Ecol. 34, 126–139. https://doi.org/10.1016/j.baae.2018.08.005 (2019).Article 

    Google Scholar 
    Turner, K. L., Conner, L. M. & Beasley, J. C. Effect of mammalian mesopredator exclusion on vertebrate scavenging communities. Sci. Rep. 10, 1–9 (2020).Article 
    CAS 

    Google Scholar 
    Ohashi, H. et al. Differences in the activity pattern of the wild boar Sus scrofa related to human disturbance. Eur. J. Wildl. Res. 59, 167–177. https://doi.org/10.1007/s10344-012-0661-z (2013).Article 

    Google Scholar 
    Saito, M. & Koike, F. Distribution of wild mammal assemblages along an urban–rural–forest landscape gradient in warm-temperate East Asia. PLoS ONE 8, e65464. https://doi.org/10.1371/journal.pone.0065464 (2013).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gaynor, K. M., Hojnowski, C. E., Carter, N. H. & Brashares, J. S. The influence of human disturbance on wildlife nocturnality. Science 360, 1232–1235. https://doi.org/10.1126/science.aar7121 (2018).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Tsunoda, M. et al. Human disturbance affects latrine-use patterns of raccoon dogs. J. Wildl. Manag. 83, 728–736. https://doi.org/10.1002/jwmg.21610 (2019).Article 

    Google Scholar 
    Watabe, R. & Saito, M. U. Effects of vehicle-passing frequency on forest roads on the activity patterns of carnivores. Landsc. Ecol. Eng. 17, 225–231. https://doi.org/10.1007/s11355-020-00434-7 (2021).Article 

    Google Scholar 
    Luna, Á., Romero-Vidal, P. & Arrondo, E. Predation and scavenging in the city: A review of spatio-temporal trends in research. Diversity 13, 46. https://doi.org/10.3390/d13020046 (2021).Article 

    Google Scholar 
    Huijbers, C. M., Schlacher, T. A., Schoeman, D. S., Weston, M. A. & Connolly, R. M. Urbanisation alters processing of marine carrion on sandy beaches. Landsc. Urban Plan. 119, 1–8 (2013).Article 

    Google Scholar 
    Fukushima Prefectural Government. Transition of evacuation designated zones. https://www.pref.fukushima.lg.jp/site/portal-english/en03-08.html. (2019). Accessed 20 Apr 2022.Steinhauser, G., Brandl, A. & Johnson, T. E. Comparison of the Chernobyl and Fukushima nuclear accidents: A review of the environmental impacts. Sci. Total Environ. 470, 800–817 (2014).ADS 
    PubMed 
    Article 
    CAS 

    Google Scholar 
    Center for International Earth Science Information Network (CIESIN)—Columbia University. (NASA Socioeconomic Data and Applications Center (SEDAC), Palisades, NY, 2018).Lyons, P. C., Okuda, K., Hamilton, M. J., Hinton, T. G. & Beasley, J. C. Rewilding of Fukushima’s human evacuation zone in the presence of radioactive stressors. Front. Ecol. Environ. 18, 127–134 (2020).Article 

    Google Scholar 
    Deryabina, T. G. et al. Long-term census data reveal abundant wildlife populations at Chernobyl. Curr. Biol. 25, R824–R826. https://doi.org/10.1016/j.cub.2015.08.017 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    Webster, S. C. et al. Where the wild things are: Influence of radiation on the distribution of four mammalian species within the Chernobyl Exclusion Zone. Front. Ecol. Environ. 14, 185–190. https://doi.org/10.1002/fee.1227 (2016).Article 

    Google Scholar 
    Schlichting, P. E., Love, C. N., Webster, S. C. & Beasley, J. C. Efficiency and composition of vertebrate scavengers at the land–water interface in the Chernobyl Exclusion Zone. Food Webs 18, e00107. https://doi.org/10.1016/j.fooweb.2018.e00107 (2019).Article 

    Google Scholar 
    Newsome, T. M. et al. Monitoring the dead as an ecosystem indicator. Ecol. Evol. 11, 5844–5856. https://doi.org/10.1002/ece3.7542 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Turner, K. L., Abernethy, E. F., Mike Conner, L., Rhodes, O. E. Jr. & Beasley, J. C. Abiotic and biotic factors modulate carrion fate and vertebrate scavenging communities. Ecology 98, 2413–2424 (2017).PubMed 
    Article 

    Google Scholar 
    Ruzicka, R. E. & Conover, M. R. Does weather or site characteristics influence the ability of scavengers to locate food?. Ethology 118, 187–196 (2012).Article 

    Google Scholar 
    Paula, J. J. S. et al. Camera-trapping as a methodology to assess the persistence of wildlife carcasses resulting from collisions with human-made structures. Wildl. Res. 41, 717–725. https://doi.org/10.1071/WR14063 (2015).Article 

    Google Scholar 
    Selva, N., Jędrzejewska, B., Jędrzejewski, W. & Wajrak, A. Factors affecting carcass use by a guild of scavengers in European temperate woodland. Can. J. Zool. 83, 1590–1601 (2005).Article 

    Google Scholar 
    Nakama, S., Yoshimura, K., Fujiwara, K., Ishikawa, H. & Iijima, K. Temporal decrease in air dose rate in the sub-urban area affected by the Fukushima Dai-ichi Nuclear Power Plant accident during four years after decontamination works. J. Environ. Radioact. 208–209, 106013. https://doi.org/10.1016/j.jenvrad.2019.106013 (2019).CAS 
    Article 
    PubMed 

    Google Scholar 
    Ministry of the Environment of Japan. Off-Site Environmental Remediation in Affected Areas in Japan. http://josen.env.go.jp/en/decontamination/ (2020). Accessed 20 Apr 2022.Japan Meteorological Agency. Climate in Namie in 2018: Monthly Overview Data. http://www.data.jma.go.jp/obd/stats/etrn/view/monthly_a1.php?prec_no=36&block_no=0295&year=2018&month=7&day=&view=p1 (2018). Accessed 1 Apr 2019.De Vault, T. L., Brisbin, J., Lehr, I., Rhodes, J. & Olin, E. Factors influencing the acquisition of rodent carrion by vertebrate scavengers and decomposers. Can. J. Zool. 82, 502–509 (2004).Article 

    Google Scholar 
    Kane, A., Healy, K., Guillerme, T., Ruxton, G. D. & Jackson, A. L. A recipe for scavenging in vertebrates—The natural history of a behaviour. Ecography 40, 11. https://doi.org/10.1111/ecog.02817 (2017).Article 

    Google Scholar 
    Natusch, D. J. D., Lyons, J. A. & Shine, R. How do predators and scavengers locate resource hotspots within a tropical forest?. Aust. Ecol. 42, 742–749. https://doi.org/10.1111/aec.12492 (2017).Article 

    Google Scholar 
    Japan Aerospace Exploration Agency. High-resolution land use land cover map of Japan (ver.16.09). https://www.eorc.jaxa.jp/ALOS/en/lulc/lulc_index.htm (2011). Accessed 1 Apr 2019.Newkirk, E. S. CPW Photo Warehouse. http://cpw.state.co.us/learn/Pages/ResearchMammalsSoftware.aspx (2016). Accessed 1 Apr 2019.Therneau, T. M. A Package for Survival Analysis in R. R package version 3.3-1 (2022).Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48. https://doi.org/10.18637/jss.v067.i01 (2015).Article 

    Google Scholar 
    Anderson, D. et al. Introgression dynamics from invasive pigs into wild boar following the March 2011 natural and anthropogenic disasters at Fukushima. Proc. R. Soc. B Biol. Sci. 288, 20210874. https://doi.org/10.1098/rspb.2021.0874 (2021).CAS 
    Article 

    Google Scholar 
    Ishiniwa, H., Onuma, M. & Tamaoki, M. Behavior of Radionuclides in the Environment III 463–472 (Springer, 2022).Book 

    Google Scholar 
    Nemoto, Y. et al. Effects of 137Cs contamination after the TEPCO Fukushima Dai-ichi Nuclear Power Station accident on food and habitat of wild boar in Fukushima Prefecture. J. Environ. Radioact. 225, 106342. https://doi.org/10.1016/j.jenvrad.2020.106342 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Olson, Z. H., Beasley, J. C. & Rhodes, O. E. Jr. Carcass type affects local scavenger guilds more than habitat connectivity. PLoS ONE 11, e0147798 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    DeVault, T. L., Seamans, T. W., Linnell, K. E., Sparks, D. W. & Beasley, J. C. Scavenger removal of bird carcasses at simulated wind turbines: Does carcass type matter?. Ecosphere. https://doi.org/10.1002/ecs2.1994 (2017).Article 

    Google Scholar 
    Sugiura, S., Tanaka, R., Taki, H. & Kanzaki, N. Differential responses of scavenging arthropods and vertebrates to forest loss maintain ecosystem function in a heterogeneous landscape. Biol. Cons. 159, 206–213 (2013).Article 

    Google Scholar 
    Enari, H. & Enari, H. S. Not avian but mammalian scavengers efficiently consume carcasses under heavy snowfall conditions: A case from northern Japan. Mamm. Biol. 101, 419–428. https://doi.org/10.1007/s42991-020-00097-9 (2021).Article 

    Google Scholar 
    Selva, N., Jedrzejewska, B., Jedrzejewski, W. & Wajrak, A. Scavenging on European bison carcasses in Bialowieza primeval forest (eastern Poland). Ecoscience 10, 303–311 (2003).Article 

    Google Scholar 
    Jojola-Elverum, S. M., Shivik, J. A. & Clark, L. Importance of bacterial decomposition and carrion substrate to foraging brown treesnakes. J. Chem. Ecol. 27, 1315–1331. https://doi.org/10.1023/a:1010357024140 (2001).CAS 
    Article 
    PubMed 

    Google Scholar 
    Abernethy, E. F., Turner, K. L., Beasley, J. C. & Rhodes, O. E. Jr. Scavenging along an ecological interface: Utilization of amphibian and reptile carcasses around isolated wetlands. Ecosphere 8, e01989. https://doi.org/10.1002/ecs2.1989 (2017).Article 

    Google Scholar 
    Sugiura, S. & Hayashi, M. Functional compensation by insular scavengers: The relative contributions of vertebrates and invertebrates vary among islands. Ecography 41, 1173–1183 (2018).Article 

    Google Scholar 
    Matsuo, R. & Ochiai, K. Dietary overlap among two introduced and one native sympatric carnivore species, the raccoon, the masked palm civet, and the raccoon dog, in Chiba Prefecture, Japan. Mammal Study 34, 187–194 (2009).Article 

    Google Scholar 
    Drygala, F. & Zoller, H. Diet composition of the invasive raccoon dog (Nyctereutes procyonoides) and the native red fox (Vulpes vulpes) in north-east Germany. Hystrix Italian J. Mammal. 24, 190–194 (2014).
    Google Scholar 
    Elmeros, M. et al. The diet of feral raccoon dog (Nyctereutes procyonoides) and native badger (Meles meles) and red fox (Vulpes vulpes) in Denmark. Mammal Res. 63, 405–413. https://doi.org/10.1007/s13364-018-0372-2 (2018).Article 

    Google Scholar 
    Sekizawa, R., Ichii, K. & Kondo, M. Satellite-based detection of evacuation-induced land cover changes following the Fukushima Daiichi nuclear disaster. Remote Sensing Lett. 6, 824–833 (2015).Article 

    Google Scholar 
    Ishihara, M. & Tadono, T. Land cover changes induced by the great east Japan earthquake in 2011. Sci. Rep. 7, 45769–45769. https://doi.org/10.1038/srep45769 (2017).ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Focardi, S., Materassi, M., Innocenti, G. & Berzi, D. Kleptoparasitism and scavenging can stabilize ecosystem dynamics. Am. Nat. 190, 398–409 (2017).PubMed 
    Article 

    Google Scholar 
    Osugi, S., Trentin, B. E. & Koike, S. Impact of wild boars on the feeding behavior of smaller frugivorous mammals. Mamm. Biol. 97, 22–27 (2019).Article 

    Google Scholar 
    Duľa, M. & Krofel, M. A cat in paradise: Hunting and feeding behaviour of Eurasian lynx among abundant naive prey. Mamm. Biol. 100, 685–690. https://doi.org/10.1007/s42991-020-00070-6 (2020).Article 

    Google Scholar 
    Smith, J. B., Laatsch, L. J. & Beasley, J. C. Spatial complexity of carcass location influences vertebrate scavenger efficiency and species composition. Sci. Rep. 7, 10250. https://doi.org/10.1038/s41598-017-10046-1 (2017).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Moleón, M. et al. Carrion availability in space and time. In Carrion Ecology and Management (eds Olea, P.P., Mateo-Tomás, P. & Sánchez-Zapata, J.A.) 23–44 (Springer International Publishing, 2019).
    DeVault, T. L. & Rhodes, O. E. Jr. Identification of vertebrate scavengers of small mammal carcasses in a forested landscape. Acta Theriol. 47, 185–192 (2002).Article 

    Google Scholar 
    Bumann, G. B. & Stauffer, D. F. Scavenging of ruffed grouse in the Appalachians: Influences and implications. Wildl. Soc. Bull. 1973–2006(30), 853–860 (2002).
    Google Scholar 
    Young, A., Stillman, R., Smith, M. J. & Korstjens, A. H. An experimental study of vertebrate scavenging behavior in a Northwest European woodland context. J. Forensic Sci. 59, 1333–1342. https://doi.org/10.1111/1556-4029.12468 (2014).Article 
    PubMed 

    Google Scholar 
    Abernethy, E. F. et al. Carcasses of invasive species are predominantly utilized by invasive scavengers in an island ecosystem. Ecosphere 7 (2016).DeVault, T. L. & Krochmal, A. R. Scavenging by snakes: An examination of the literature. Herpetologica 58, 429–436 (2002).Article 

    Google Scholar 
    Shivik, J. A. & Clark, L. Ontogenetic shifts in carrion attractiveness to brown tree snakes (Boiga irregularis). J. Herpetol. 33, 334–336. https://doi.org/10.2307/1565737 (1999).Article 

    Google Scholar 
    Campobasso, C. P., Di Vella, G. & Introna, F. Factors affecting decomposition and Diptera colonization. Forensic Sci. Int. 120, 18–27 (2001).CAS 
    PubMed 
    Article 

    Google Scholar  More