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    Spatial genetic structure of European wild boar, with inferences on late-Pleistocene and Holocene demographic history

    Ai H, Fang X, Yang B, Huang Z, Chen H, Mao L et al. (2015) Adaptation and possible ancient interspecies introgression in pigs identified by whole-genome sequencing. Nat Genet 47:217–225Article 
    CAS 

    Google Scholar 
    Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19:1655–1664Article 
    CAS 

    Google Scholar 
    Alexandri P, Megens HJ, Crooijmans RPMA, Groenen MAM, Goedbloed DJ, Herrero-Medrano JM et al. (2017) Distinguishing migration events of different timing for wild boar in the Balkans. J Biogeogr 44:259–270Article 

    Google Scholar 
    Alexandri P, Triantafyllidis A, Papakostas S, Chatzinikos E, Platis P, Papageorgiou N et al. (2012) The Balkans and the colonization of Europe: the post-glacial range expansion of the wild boar, Sus scrofa. J Biogeogr 39:713–723Article 

    Google Scholar 
    Alves PC, Pinheiro I, Godinho R, Vicente JJ, Gortázar C, Scandura M et al. (2010) Genetic diversity of wild boar populations and domestic pig breeds (Sus scrofa) in South-western Europe. Biol J Linn Soc 101:797–822Article 

    Google Scholar 
    Apollonio M, Andersen R, Putman R (2010) European ungulates and their management in the 21st century (M Apollonio, R Andersen, and R Putman, Eds.) Cambridge University Press: Cambridge, UKAzzaroli A, De Giuli C, Ficcarelli G, Torre D (1988) Late pliocene to early mid-pleistocene mammals in Eurasia: Faunal succession and dispersal events. Palaeogeogr Palaeoclimatol Palaeoecol 66:77–100Article 

    Google Scholar 
    Bérénos C, Ellis PA, Pilkington JG, Pemberton JM (2016) Genomic analysis reveals depression due to both individual and maternal inbreeding in a free‐living mammal population. Mol Ecol 25:3152–3168Article 

    Google Scholar 
    Braga RT, Rodrigues JFM, Diniz-Filho JAF, Rangel TF (2019) Genetic population structure and allele surfing during range expansion in dynamic habitats. An da Academia Brasileira de Ciências 91:e20180179Article 

    Google Scholar 
    Bragina EV, Ives AR, Pidgeon AM, Kuemmerle T, Baskin LM, Gubar YP, Piquer-Rodríguez M, Keuler NS, Petrosyan VG, Radeloff VC (2015) Rapid Declines of Large Mammal Populations after the Collapse of the Soviet Union. Cons Biol 29:844–853Article 

    Google Scholar 
    Brewer S, Cheddadi R, de Beaulieu JL, Reille M, Allen J, Almqvist-Jacobson H et al. (2002) The spread of deciduous Quercus throughout Europe since the last glacial period. For Ecol Manag 156:27–48Article 

    Google Scholar 
    Cahill S, Llimona F, Cabañeros L, Calomardo F (2012) Characteristics of wild boar (Sus scrofa) habituation to urban areas in the Collserola Natural Park (Barcelona) and comparison with other locations. Anim Biodivers Conserv 35:221–233Article 

    Google Scholar 
    Canu A, Costa S, Iacolina L, Piatti P, Apollonio M, Scandura M (2014) Are captive wild boar more introgressed than free-ranging wild boar? Two case studies in Italy. Eur J Wildl Res 60:459–467Article 

    Google Scholar 
    Canu A, Vilaça STT, Iacolina L, Apollonio M, Bertorelle G, Scandura M (2016) Lack of polymorphism at the MC1R wild-type allele and evidence of domestic allele introgression across European wild boar populations. Mamm Biol 81:477–479Article 

    Google Scholar 
    Carranza J, Salinas M, de Andrés D, Pérez-González J (2016) Iberian red deer: paraphyletic nature at mtDNA but nuclear markers support its genetic identity. Ecol Evol 6:905–922Article 

    Google Scholar 
    Chang CC, Chow CC, Tellier LCAM, Vattikuti S, Purcell SM, Lee JJ (2015) Second-generation PLINK: Rising to the challenge of larger and richer datasets. Gigascience 4:1–16Article 

    Google Scholar 
    Cheddadi R, Bar-Hen A (2009) Spatial gradient of temperature and potential vegetation feedback across Europe during the late Quaternary. Clim Dyn 32:371–379Article 

    Google Scholar 
    Clark PU, Dyke AS, Shakun JD, Carlson AE, Clark J, Wohlfarth B et al. (2009) The Last Glacial Maximum. Science 325:710–714Article 
    CAS 

    Google Scholar 
    DeGiorgio M, Rosenberg NA (2013) Geographic sampling scheme as a determinant of the major axis of genetic variation in principal components analysis. Mol Biol Evol 30:480–488Article 
    CAS 

    Google Scholar 
    Deinet S, Ieronymidou C, McRae L, Burfield IJ, Foppen RP, Collen B, et al. (2013) Wildlife comeback in Europe. The recovery of selected mammal and bird species. London, UKEckert CG, Samis KE, Lougheed SC (2008) Genetic variation across species’ geographical ranges: the central–marginal hypothesis and beyond. Mol Ecol 17:1170–1188Article 
    CAS 

    Google Scholar 
    Fang M, Berg F, Ducos A, Andersson L (2006) Mitochondrial haplotypes of European wild boars with 2n = 36 are closely related to those of European domestic pigs with 2n = 38. Anim Genet 37:459–464Article 
    CAS 

    Google Scholar 
    Ferenčaković M, Sölkner J, Curik I (2013) Estimating autozygosity from high-throughput information: Effects of SNP density and genotyping errors. Genet Sel Evol 45:42Article 

    Google Scholar 
    Ferreira E, Souto L, Soares AMVM, Fonseca C (2009) Genetic structure of the wild boar population in Portugal: Evidence of a recent bottleneck. Mamm Biol 74:274–285Article 

    Google Scholar 
    Franois O, Currat M, Ray N, Han E, Excoffier L, Novembre J (2010) Principal component analysis under population genetic models of range expansion and admixture. Mol Biol Evol 27:1257–1268Article 

    Google Scholar 
    Frantz AC, Bertouille S, Eloy MC, Licoppe A, Chaumont F, Flamand MC (2012) Comparative landscape genetic analyses show a Belgian motorway to be a gene flow barrier for red deer (Cervus elaphus), but not wild boars (Sus scrofa). Mol Ecol 21:3445–3457Article 
    CAS 

    Google Scholar 
    Fulgione D, Rippa D, Buglione M, Trapanese M, Petrelli S, Maselli V (2016) Unexpected but welcome. Artificially selected traits may increase fitness in wild boar. Evol Appl 9:769–776Article 
    CAS 

    Google Scholar 
    Goedbloed DJ, Megens HJ, van Hooft P, Herrero-Medrano JM, Lutz W, Alexandri P et al. (2013a) Genome-wide single nucleotide polymorphism analysis reveals recent genetic introgression from domestic pigs into Northwest European wild boar populations. Mol Ecol 22:856–866Article 
    CAS 

    Google Scholar 
    Goedbloed DJ, van Hooft P, Megens HJ, Langenbeck K, Lutz W, Crooijmans RPMA et al. (2013b) Reintroductions and genetic introgression from domestic pigs have shaped the genetic population structure of Northwest European wild boar. BMC Genet 14:2–10Article 

    Google Scholar 
    Groenen MAM, Archibald AL, Uenishi H, Tuggle CK, Takeuchi Y, Rothschild MF et al. (2012) Analyses of pig genomes provide insight into porcine demography and evolution. Nature 491:393–398Article 
    CAS 

    Google Scholar 
    Herrero-Medrano JM, Megens H-J, Groenen MAM, Ramis G, Bosse M, Pérez-Enciso M et al. (2013) Conservation genomic analysis of domestic and wild pig populations from the Iberian Peninsula. BMC Genet 14:1–13Article 

    Google Scholar 
    Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112Article 

    Google Scholar 
    Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Philos Trans R Soc Lond Ser B Biol Sci 359:183–195Article 
    CAS 

    Google Scholar 
    Hiemstra PH, Pebesma EJ, Twenhöfel CJW, Heuvelink GBM (2009) Real-time automatic interpolation of ambient gamma dose rates from the Dutch radioactivity monitoring network. Comput Geosci 35:1711–1721Article 
    CAS 

    Google Scholar 
    Howrigan DP, Simonson MA, Keller MC (2011) Detecting autozygosity through runs of homozygosity: a comparison of three autozygosity detection algorithms. BMC Genomics 12:460Article 
    CAS 

    Google Scholar 
    Huisman J, Kruuk LEB, Ellis PA, Clutton-Brock T, Pemberton JM (2016) Inbreeding depression across the lifespan in a wild mammal population. Proc Natl Acad Sci 113:3585–3590Article 
    CAS 

    Google Scholar 
    Iacolina L, Corlatti L, Buzan E, Safner T, Šprem N (2019) Hybridisation in European ungulates: an overview of the current status, causes, and consequences. Mamm Rev 49:45–59Article 

    Google Scholar 
    Iacolina L, Pertoldi C, Amills M, Kusza S, Megens H-J, Bâlteanu VA et al. (2018) Hotspots of recent hybridization between pigs and wild boars in Europe. Sci Rep. 8:17372Article 
    CAS 

    Google Scholar 
    Iacolina L, Scandura M, Goedbloed DJ, Alexandri P, Crooijmans RPMA, Larson G et al. (2016) Genomic diversity and differentiation of a managed island wild boar population. Heredity 116:60–67Article 
    CAS 

    Google Scholar 
    Jombart T, Ahmed I (2011) adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27:1–2Article 

    Google Scholar 
    de Jong JF, Hooft van P, Megens HJ, Crooijmans RPMA, Groot de GA, Pemberton JM, Huisman J et al. (2020) Fragmentation and translocation distort the genetic landscape of ungulates: red deer in the Netherlands. Front Ecol Evol 8:535715Article 

    Google Scholar 
    Kamvar ZN, Tabima JF, Grünwald NJ (2014) Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2:e281Article 

    Google Scholar 
    Kardos M, Åkesson M, Fountain T, Flagstad Ø, Liberg O, Olason P et al. (2018) Genomic consequences of intensive inbreeding in an isolated wolf population. Nat Ecol Evol 2:124–131Article 

    Google Scholar 
    Kaplan JO, Krumhardt KM, Zimmermann N (2009) The prehistoric and preindustrial deforestation of Europe. Quat Sci Rev 28:3016–3034. https://doi.org/10.1016/j.quascirev.2009.09.028Koemle D, Zinngrebe Y, Yu X (2018) Highway construction and wildlife populations: Evidence from Austria. Land use policy 73:447–457Article 

    Google Scholar 
    Krže B (1982) Divji prašič: biologija, gojitev, ekologija. Lovska zveza Slovenije, Ljubljana
    Google Scholar 
    Kusza S, Podgórski T, Scandura M, Borowik T, Jávor A, Sidorovich VE et al. (2014) Contemporary genetic structure, phylogeography and past demographic processes of wild boar Sus scrofa population in central and eastern Europe. PLoS One 9:e91401Article 

    Google Scholar 
    Lorenzini R, Lovari S, Masseti M (2002) The rediscovery of the Italian roe deer: Genetic differentiation and management implications. Ital J Zool 69(4):367–379Article 

    Google Scholar 
    Lorenzini R, San José C, Braza F, Aragón S (2003) Genetic differentiation and phylogeography of roe deer in Spain, as suggested by mitochondrial DNA and microsatellite analysis. Ital J Zool 70(1):89–99Article 
    CAS 

    Google Scholar 
    Magri D (2013) Early to Middle Pleistocene dynamics of plant and mammal communities in South West Europe. Quat Int 288:63–72Article 

    Google Scholar 
    Manunza A, Zidi A, Yeghoyan S, Balteanu VA, Carsai TC, Scherbakov O et al. (2013) A high throughput genotyping approach reveals distinctive autosomal genetic signatures for European and Near Eastern wild boar. PLoS One 8:e55891Article 
    CAS 

    Google Scholar 
    Maselli V, Rippa D, De Luca A, Larson G, Wilkens B, Linderholm A et al. (2016) Southern Italian wild boar population, hotspot of genetic diversity. Hystrix 27:137–144
    Google Scholar 
    McVean G (2009) A genealogical interpretation of principal components analysis. PLoS Genet 5:e1000686Article 

    Google Scholar 
    Megens H-J, Crooijmans RP, Cristobal M, Hui X, Li N, Groenen MA (2008) Biodiversity of pig breeds from China and Europe estimated from pooled DNA samples: differences in microsatellite variation between two areas of domestication. Genet Sel Evol 40:103
    Google Scholar 
    Melis C, Szafrańska PA, Jȩdrzejewska B, Bartoń K (2006) Biogeographical variation in the population density of wild boar (Sus scrofa) in western Eurasia. J Biogeogr 33:803–811Article 

    Google Scholar 
    Mihalik B, Stéger V, Frank K, Szendrei L, Kusza S (2018) Barrier effect of the M3 highway in Hungary on the genetic diversity of wild boar (Sus scrofa) population. Res J Biotechnol 13:32–38
    Google Scholar 
    NCBI (2018) Genome Organism Overview: Sus scrofa (pig). https://www.ncbi.nlm.nih.gov/genome?term=sus%20scrofa%20%5BOrganism%5D&cmd=DetailsSearch&report=OverviewNikolov IS, Gum B, Markov G, Kuehn R (2009) Population genetic structure of wild boar Sus scrofa in Bulgaria as revealed by microsatellite analysis. Acta Theriol (Warsz) 54:193–205Article 

    Google Scholar 
    Nykänen M, Rogan E, Foote AD, Kaschner K, Dabin W, Louis M et al. (2019) Postglacial colonization of northern coastal habitat by bottlenose dolphins: a marine leading-edge expansion? J Hered 110:662–674Article 

    Google Scholar 
    Palombo M, Romana AV-G (2003) Remarks on the biochronology of mammalian faunal complexes from the Pliocene to the Middle Pleistocene in France. Geol Rom: 145–163Paradis E, Claude J, Strimmer K (2004) APE: analysis of phylogenetics and evolution in R language. Bioinformatics 20:289–290Article 
    CAS 

    Google Scholar 
    Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D et al (2007) PLINK: A tool Set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559–575. www.cog-genomics.org/plink/1.9/Putman R, Apollonio M, Andersen R (2011) Ungulate management in Europe: problems and practices. Cambridge University Press, Cambridge, UKBook 

    Google Scholar 
    R Core Team (2018) R: A language and environment for statistical computing. Vienna, AustriaRejduch B, Sota E, Ró M, Ko M (2003) Chromosome number polymorphism in a litter of European wild boar (Sus scrofa scrofa L.). Anim Sci Pap Rep. 21:57–62
    Google Scholar 
    Scandura M, Iacolina L, Apollonio M (2011a) Genetic diversity in the European wild boar Sus scrofa: phylogeography, population structure and wild x domestic hybridization: Genetic variation in European wild boar. Mamm Rev 41:125–137Article 

    Google Scholar 
    Scandura M, Iacolina L, Cossu A, Apollonio M (2011b) Effects of human perturbation on the genetic make-up of an island population: The case of the Sardinian wild boar. Heredity 106:1012–1020Article 
    CAS 

    Google Scholar 
    Scandura M, Iacolina L, Crestanello B, Pecchioli E, Di Benedetto MF, Russo V et al. (2008) Ancient vs. recent processes as factors shaping the genetic variation of the European wild boar: Are the effects of the last glaciation still detectable? Mol Ecol 17:1745–1762Article 
    CAS 

    Google Scholar 
    Scandura M, Fabbri G, Caniglia R, Iacolina L, Mattucci F, Mengoni C, Pante G, Apollonio M, Mucci N (2022) Resilience to Historical Human Manipulations in the Genomic Variation of Italian Wild Boar Populations. Front Ecol Evol 10:833081Article 

    Google Scholar 
    Schmitt T, Varga Z (2012) Extra-Mediterranean refugia: the rule and not the exception. Front Zool 9:22Article 

    Google Scholar 
    Sommer RS, Fahlke JM, Schmölcke U, Benecke N, Zachos FE (2009) Quaternary history of the European roe deer Capreolus capreolus. Mamm Rev 39:1–16Article 

    Google Scholar 
    Sommer RS, Nadachowski A (2006) Glacial refugia of mammals in Europe: evidence from fossil records. Mamm Rev 36:251–265Article 

    Google Scholar 
    Sommer RS, Zachos FE (2009) Fossil evidence and phylogeography of temperate species: ‘glacial refugia’ and post-glacial recolonization. J Biogeogr 36:2013–2020Article 

    Google Scholar 
    Sommer RS, Zachos FE, Street M, Jöris O, Skog A, Benecke N (2008) Late Quaternary distribution dynamics and phylogeography of the red deer (Cervus elaphus) in Europe. Quat Sci Rev 27:714–733Article 

    Google Scholar 
    Stillfried M, Fickel J, Börner K, Wittstatt U, Heddergott M, Ortmann S et al. (2017) Do cities represent sources, sinks or isolated islands for urban wild boar population structure? J Appl Ecol 54:272–281Article 

    Google Scholar 
    Taberlet P, Fumagalli L, Wust-Saucy AG, Cossons JF (1998) Comparative phylogeography and post-glacial colonization routes in Europe. Mol Ecol 7:453–461.Article 
    CAS 

    Google Scholar 
    Veličković N, Djan M, Ferreira E, Stergar M, Obreht D, Maletić V et al. (2015) From north to south and back: the role of the Balkans and other southern peninsulas in the recolonization of Europe by wild boar. J Biogeogr 42:716–728Article 

    Google Scholar 
    Veličković N, Ferreira E, Djan M, Ernst M, Obreht Vidaković D, Monaco A et al. (2016) Demographic history, current expansion and future management challenges of wild boar populations in the Balkans and Europe. Heredity 117:348–357Article 

    Google Scholar 
    Vernesi C, Crestanello B, Pecchioli E, Tartari D, Caramelli D, Hauffe H et al. (2003) The genetic impact of demographic decline and reintroduction in the wild boar (Sus scrofa): A microsatellite analysis. Mol Ecol 12:585–595Article 
    CAS 

    Google Scholar 
    Vilaça ST, Biosa D, Zachos F, Iacolina L, Kirschning J, Alves PC et al. (2014) Mitochondrial phylogeography of the European wild boar: The effect of climate on genetic diversity and spatial lineage sorting across Europe. J Biogeogr 41:987–998Article 

    Google Scholar 
    Zachos FE, Frantz AC, Kuehn R, Bertouille S, Colyn M, Niedziałkowska M et al. (2016) Genetic structure and effective population sizes in European red deer (Cervus elaphus) at a continental scale: insights from microsatellite DNA. J Hered 107:318–326 More

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    Global patterns of climate change impacts on desert bird communities

    Parmesan, C. & Yohe, G. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42 (2003).Article 
    ADS 
    CAS 

    Google Scholar 
    Chen, I.-C., Hill, J. K., Ohlemüller, R., Roy, D. B. & Thomas, C. D. Rapid range shifts of species associated with high levels of climate warming. Science 333, 1024–1026 (2011).Article 
    ADS 
    CAS 

    Google Scholar 
    Bowler, D. E. et al. Cross-realm assessment of climate change impacts on species’ abundance trends. Nat. Ecol. Evol. 1, 1–7 (2017).Article 

    Google Scholar 
    Barrett, J. E. et al. Persistent effects of a discrete warming event on a polar desert ecosystem. Glob. Change Biol. 14, 2249–2261 (2008).Article 
    ADS 

    Google Scholar 
    Gooseff, M. N. et al. Decadal ecosystem response to an anomalous melt season in a polar desert in Antarctica. Nat. Ecol. Evol. 1, 1334–1338 (2017).Article 

    Google Scholar 
    Iknayan, K. J. & Beissinger, S. R. In transition: Avian biogeographic responses to a century of climate change across desert biomes. Glob. Change Biol. 26, 3268–3284 (2020).Article 
    ADS 

    Google Scholar 
    Conradie, S. R., Woodborne, S. M., Cunningham, S. J. & McKechnie, A. E. Chronic, sublethal effects of high temperatures will cause severe declines in southern African arid-zone birds during the 21st century. Proc. Natl Acad. Sci. USA 116, 14065–14070 (2019).Article 
    ADS 
    CAS 

    Google Scholar 
    du Plessis, K. L., Martin, R. O., Hockey, P. A. R., Cunningham, S. J. & Ridley, A. R. The costs of keeping cool in a warming world: implications of high temperatures for foraging, thermoregulation and body condition of an arid-zone bird. Glob. Change Biol. 18, 3063–3070 (2012).Article 
    ADS 

    Google Scholar 
    Ward, D. The Biology of Deserts (OUP Oxford, 2016).Reid, V. W. et al. Millennium Ecosystem Assessment, 2005. In Ecosystems and Human Well-being: Synthesis (Island Press, 2005).Zhou, L., Chen, H. & Dai, Y. Stronger warming amplification over drier ecoregions observed since 1979. Environ. Res. Lett. 10, 064012 (2015).Article 
    ADS 

    Google Scholar 
    Hoegh-Guldberg, O. et al. 2018: Impacts of 1.5ºC Global Warming on Natural and Human Systems. In: Global Warming of 1.5°C. An IPCC Special Report on the impacts of global warming of 1.5°C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty (eds Masson-Delmotte, V. et al.) Cambridge University Press, Cambridge, UK and New York, NY, USA, pp. 175-312, https://doi.org/10.1017/9781009157940.005.Albright, T. P. et al. Mapping evaporative water loss in desert passerines reveals an expanding threat of lethal dehydration. Proc. Natl Acad. Sci. USA 114, 2283–2288 (2017).Article 
    ADS 
    CAS 

    Google Scholar 
    Friedrich, T., Timmermann, A., Tigchelaar, M., Timm, O. E. & Ganopolski, A. Nonlinear climate sensitivity and its implications for future greenhouse warming. Sci. Adv. 2, e1501923 (2016).Article 
    ADS 

    Google Scholar 
    Kearney, M. R. & Porter, W. P. NicheMapR—an R package for biophysical modelling: the microclimate model. Ecography 40, 664–674 (2017).Article 

    Google Scholar 
    Huey, R. B. et al. Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 367, 1665–1679 (2012).Article 

    Google Scholar 
    Kearney, M. & Porter, W. Mechanistic niche modelling: combining physiological and spatial data to predict species’ ranges. Ecol. Lett. 12, 334–350 (2009).Article 

    Google Scholar 
    Bicudo, J. E. P., Buttemer, W. A., Chappell, M. A., Pearson, J. T. & Bech, C. Ecological and Environmental Physiology of Birds Vol. 2 (Oxford University Press, 2010).McKechnie, A. E. & Wolf, B. O. Climate change increases the likelihood of catastrophic avian mortality events during extreme heat waves. Biol. Lett. 6, 253–256 (2010).Article 

    Google Scholar 
    Riddell, E. A. et al. Exposure to climate change drives stability or collapse of desert mammal and bird communities. Science 371, 633–636 (2021).Article 
    ADS 
    CAS 

    Google Scholar 
    Williams, J. B. & Tieleman, B. I. Physiological adaptation in desert birds. BioScience 55, 416–425 (2005).Article 

    Google Scholar 
    Iknayan, K. J. & Beissinger, S. R. Collapse of a desert bird community over the past century driven by climate change. Proc. Natl Acad. Sci. USA 115, 8597–8602 (2018).Article 
    ADS 
    CAS 

    Google Scholar 
    Albright, T. P. et al. Combined effects of heat waves and droughts on avian communities across the conterminous United States. Ecosphere 1, art12 (2010).Article 

    Google Scholar 
    Cruz-McDonnell, K. K. & Wolf, B. O. Rapid warming and drought negatively impact population size and reproductive dynamics of an avian predator in the arid southwest. Glob. Change Biol. 22, 237–253 (2016).Article 
    ADS 

    Google Scholar 
    Dawson, W. R. Temperature Regulation and Water Requirements of the Brown and Abert Towhees, Pipilo Fuscus and Pipilo Aberti.[With Plates.] (University of California Press, 1954).Riddell, E. A., Iknayan, K. J., Wolf, B. O., Sinervo, B. & Beissinger, S. R. Cooling requirements fueled the collapse of a desert bird community from climate change. Proc. Natl. Acad. Sci. USA https://doi.org/10.1073/pnas.1908791116 (2019).Wolf, B. Global warming and avian occupancy of hot deserts; a physiological and behavioral perspective. Rev. Chil. Hist. Nat. 73, 395–400 (2000).Article 

    Google Scholar 
    Kier, G. et al. A global assessment of endemism and species richness across island and mainland regions. Proc. Natl Acad. Sci. USA 106, 9322–9327 (2009).Article 
    ADS 
    CAS 

    Google Scholar 
    Ioffe, S. Improved consistent sampling, weighted Minhash and L1 sketching. In Proceedings of the 2010 IEEE International Conference on Data Mining 246–255 (IEEE Computer Society, 2010).Losos, E., Hayes, J., Phillips, A., Wilcove, D. & Alkire, C. Taxpayer-subsidized resource extraction harms species. BioScience 45, 446–455 (1995).Article 

    Google Scholar 
    Rodríguez-Estrella, R. Land use changes affect distributional patterns of desert birds in the Baja California peninsula, Mexico. Divers. Distrib. 13, 877–889 (2007).Article 

    Google Scholar 
    Stralberg, D. et al. Climate-change refugia in boreal North America: what, where, and for how long? Front. Ecol. Environ. 18, 261–270 (2020).Article 

    Google Scholar 
    Hinkel, J. et al. Sea-level rise scenarios and coastal risk management. Nat. Clim. Change 5, 188–190 (2015).Article 
    ADS 

    Google Scholar 
    He, Q. & Silliman, B. R. Climate change, human impacts, and coastal ecosystems in the anthropocene. Curr. Biol. 29, R1021–R1035 (2019).Article 
    CAS 

    Google Scholar 
    C. B. D. Zero Draft of the Post-2020 Global Biodiversity Framework CBD/WG2020/2/3. https://www.cbd.int/doc/c/efb0/1f84/a892b98d2982a829962b6371/wg2020-02-03-en.pdf Convention on Biology Diversity, Montreal, Canada (2020).Jung, M. et al. A global map of terrestrial habitat types. Sci. Data 7, 256 (2020).Article 

    Google Scholar 
    Fick, S. E. & Hijmans, R. J. WorldClim 2: new 1 km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).Article 

    Google Scholar 
    Meigs, P. World distributions of arid and semi-arid homoclimates. In Review of Research on Arid Zone Hydrology (UNESCO, 1953).Holt, B. G. et al. An update of Wallace’s zoogeographic regions of the world. Science 339, 74–78 (2013).Article 
    ADS 
    CAS 

    Google Scholar 
    Abatzoglou, J. T., Dobrowski, S. Z., Parks, S. A. & Hegewisch, K. C. TerraClimate, a high-resolution global dataset of monthly climate and climatic water balance from 1958-2015. Sci. Data 5, 170191 (2018).Article 

    Google Scholar 
    Qin, Y. et al. Agricultural risks from changing snowmelt. Nat. Clim. Change 10, 459–465 (2020).Article 
    ADS 

    Google Scholar 
    Kearney, M. R. & Porter, W. P. NicheMapR – an R package for biophysical modelling: the microclimate model. Ecography 40, 664–674 (2017).Article 

    Google Scholar 
    Pattinson, N. B. et al. Heat dissipation behaviour of birds in seasonally hot arid-zones: are there global patterns? J. Avian Biol. 51, e02350 (2020).Smith, E. K., O’Neill, J., Gerson, A. R. & Wolf, B. O. Avian thermoregulation in the heat: resting metabolism, evaporative cooling and heat tolerance in Sonoran Desert doves and quail. J. Exp. Biol. 218, 3636–3646 (2015).Article 

    Google Scholar 
    Smith, E. K., O’Neill, J. J., Gerson, A. R., McKechnie, A. E. & Wolf, B. O. Avian thermoregulation in the heat: resting metabolism, evaporative cooling and heat tolerance in Sonoran Desert songbirds. J. Exp. Biol. 220, 3290–3300 (2017).
    Google Scholar 
    Kearney, M. NicheMapR: R implementation of Niche Mapper software for biophysical modelling. https://github.com/mrke/NicheMapR. (2020).Cunningham, S. J., Martin, R. O. & Hockey, P. A. Can behaviour buffer the impacts of climate change on an arid-zone bird? Ostrich 86, 119–126 (2015).Article 

    Google Scholar 
    Czenze, Z. J. et al. Regularly drinking desert birds have greater evaporative cooling capacity and higher heat tolerance limits than non-drinking species. Funct. Ecol. 34, 1589–1600 (2020).Article 

    Google Scholar 
    Smit, B. et al. Avian thermoregulation in the heat: phylogenetic variation among avian orders in evaporative cooling capacity and heat tolerance. J. Exp. Biol. 221, jeb174870 (2018).Worcester, S. E. The scaling of the size and stiffness of primary flight feathers. J. Zool. 239, 609–624 (1996).Article 

    Google Scholar 
    Wang, X., Nudds, R. L., Palmer, C. & Dyke, G. J. Size scaling and stiffness of avian primary feathers: implications for the flight of Mesozoic birds. J. Evol. Biol. 25, 547–555 (2012).Article 
    CAS 

    Google Scholar 
    McKechnie, A. E., Gerson, A. R. & Wolf, B. O. Thermoregulation in desert birds: scaling and phylogenetic variation in heat tolerance and evaporative cooling. J. Exp. Biol. 224, jeb229211 (2021).Flint, L. E., Flint, A. L., Thorne, J. H. & Boynton, R. Fine-scale hydrologic modeling for regional landscape applications: the California Basin Characterization Model development and performance. Ecol. Process. 2, 25 (2013).Article 

    Google Scholar 
    Handbook of the Birds of the World and BirdLife International. Handbook of the Birds of the World and BirdLife International digital checklist of the birds of the world. Version 5. http://datazone.birdlife.org/userfiles/file/Species/Taxonomy/HBW-BirdLife_Checklist_v5_Dec20.zip (2020).Brooks, T. M. et al. Measuring terrestrial Area of Habitat (AOH) and its utility for the IUCN red list. Trends Ecol. Evol. 34, 977–986 (2019).Article 

    Google Scholar 
    Pastore, M. Overlapping: a R package for estimating overlapping in empirical distributions. J. Open Source Softw. 3, 1023 (2018).Article 
    ADS 

    Google Scholar 
    UNEP-WCMC and IUCN, Protected Planet: The World Database on Protected Areas (WDPA) [Online], June 2021, Cambridge, UK: UNEP-WCMC and IUCN www.protectedplanet.net (2021).Butchart, S. H. M. et al. Shortfalls and solutions for meeting national and global conservation area targets. Conserv. Lett. 8, 329–337 (2015).Article 

    Google Scholar 
    Dudley, N. Guidelines for Applying Protected Area Management Categories (ICUN, 2008).Mangiafico, S. rcompanion: Functions to Support Extension Education Program Evaluation. https://CRAN.R-project.org/package=rcompanion. (2021).Crawford, C. L., Estes, L. D., Searchinger, T. D. & Wilcove, D. S. Consequences of underexplored variation in biodiversity indices used for land-use prioritization. Ecol. Appl. 31, e02396 (2021).Article 

    Google Scholar 
    Gorelick, N. et al. Google Earth Engine: planetary-scale geospatial analysis for everyone. Remote Sens. Environ. 202, 18–27 (2017).Article 
    ADS 

    Google Scholar 
    R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2020). More

  • in

    Partial COVID-19 closure of a national park reveals negative influence of low-impact recreation on wildlife spatiotemporal ecology

    Laundré, J. W., Hernández, L. & Altendorf, K. B. Wolves, elk, and bison: reestablishing the “landscape of fear” in Yellowstone National Park, U.S.A.. Can. J. Zool. 79, 1401–1409 (2001).Article 

    Google Scholar 
    Laundré, J. W., Hernandez, L. & Ripple, W. J. The landscape of fear: Ecological implications of being afraid. Open Ecol. J. 3, 1–7 (2010).Article 

    Google Scholar 
    Suraci, J. P., Clinchy, M., Zanette, L. Y. & Wilmers, C. C. Fear of humans as apex predators has landscape-scale impacts from mountain lions to mice. Ecol. Lett. 22, 1578–1586 (2019).Article 

    Google Scholar 
    Miller, S. G., Knight, R. L. & Miller, C. K. Wildlife responses to pedestrians and dogs. Wildl. Soc. B. 29, 124–132 (2001).
    Google Scholar 
    Larson, C., Reed, S., Merenlender, A. M. & Crooks, K. R. Effects of recreation on animals revealed as widespread through a global systemic review. PLoS ONE 11, 1–21 (2016).Article 

    Google Scholar 
    Balmford, A. et al. Walk on the wild side: Estimating the global magnitude of visits to protected areas. PLoS Biol 13, 1–6 (2015).Article 

    Google Scholar 
    Baker, A. D. & Leberg, P. L. Impacts of human recreation on carnivores in protected areas. PLoS Biol 13, 1–21 (2018).
    Google Scholar 
    Schulze, K. et al. An assessment of threats to terrestrial protected areas. Cons. Lett. 11, 1–10 (2018).Article 

    Google Scholar 
    Suraci, J. P. et al. Disturbance type and species life history predict mammal responses to humans. Glob. Change Biol. 27, 3718–3731 (2021).Article 
    CAS 

    Google Scholar 
    Reilly, M. L., Tobler, M. W., Sonderegger, D. L. & Beier, P. Spatial and temporal response of wildlife to recreational activities in the San Francisco Bay ecoregion. Biol. Conserv. 207, 117–126 (2017).Article 

    Google Scholar 
    Naidoo, R. & Burton, A. C. Relative effects of recreational activities on a temperate terrestrial wildlife assemblage. Conserv. Sci. Pract. 2, e271 (2020).
    Google Scholar 
    Nickel, B. A., Suraci, J. P., Allen, M. L. & Wilmers, C. C. Human presence and human footprint have non-equivalent effects on wildlife spatiotemporal habitat use. Biol. Conserv. 241, 1–11 (2020).Article 

    Google Scholar 
    Blanchet, F. G., Cazelles, K. & Gravel, D. Co-occurrence is not evidence of ecological interactions. Ecol. Lett. 23, 1050–1063 (2020).Article 

    Google Scholar 
    Poggiato, G. et al. On the interpretations of joint modeling in community ecology. TREE 36, 391–401 (2021).
    Google Scholar 
    Bates, A. E., Primack, R. B., Moraga, P. & Duarte, C. M. COVID-19 pandemic and associated lockdown as a “Global Human Confinement Experiment” to investigate biodiversity conservation. Biol. Conserv. 248, 1–6 (2020).Article 

    Google Scholar 
    Rutz, C. et al. COVID-19 lockdown allows researchers to quantify the effects of human activity on wildlife. Nat. Ecol. Evol. 4, 1156–1159 (2020).Article 

    Google Scholar 
    Wang, Y., Allen, M. L. & Wilmers, C. C. Mesopredator spatial and temporal responses to large predators and human development in the Santa Cruz Mountains of California. Biol. Conserv. 190, 23–33 (2015).Article 

    Google Scholar 
    Lewis, J. S. et al. Human activity influences wildlife populations and activity patterns: implications for spatial and temporal refuges. Ecosphere 12, 1–16 (2021).Article 

    Google Scholar 
    Corradini, A. et al. Effects of cumulated outdoor activity on wildlife habitat use. Biol. Conserv. 253, 108818 (2021).Article 

    Google Scholar 
    Soule, M. E. et al. Dynamics of rapid extinctions of chaparral-requiring birds in urban habitat islands. Conserv. Biol. 2, 75–92 (1988).Article 

    Google Scholar 
    Feit, B., Feit, A. & Letnic, M. Apex predators decouple population dynamics between mesopredators and their prey. Ecosystems 22, 1606–1617 (2019).Article 

    Google Scholar 
    Berger, J. Fear, human shields and the redistribution of prey and predators in protected areas. Biol. Lett. 3, 620–623 (2007).Article 

    Google Scholar 
    Sarmento, W., Biel, M. & Berger, J. Redistribution, human shields and loss of migratory behavior in the crown of the continent. Intermt. J. Sci. 22, 2016 (2016).
    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 (2018).Article 
    ADS 
    CAS 

    Google Scholar 
    Microsoft. AI for Earth camera trap image processing API (2020).Niedballa, J., Sollmann, R., Courtiol, A. & Wilting, A. camtrapR: an R package for efficient camera trap data management. Methods Ecol. Evol. 7, 1457–1462 (2016).Article 

    Google Scholar 
    MacKenzie, D. I., Nichols, J. D., Hines, J. E., Knutson, M. G. & Franklin, A. B. Estimating site occupancy, colonization, and local extinction when a species is detected imperfectly. Ecology 84, 2200–2207. https://doi.org/10.1890/02-3090 (2003).Article 

    Google Scholar 
    MacKenzie, D. I. et al. Occupancy estimation and modeling (Elsevier, 2018).
    Google Scholar 
    Fiske, I. & Chandler, R. unmarked: An R package for fitting hierarchical models of wildlife occurrence and abundance. J. Stat. Soft. 4, 1–23 (2011).
    Google Scholar 
    Mazerolle, M. J. AICcmodavg: Model selection and multimodel inference based on (Q)AIC(c). R package version 2.3-1 (2020). https://cran.r-project.org/package=AICcmodavg.Ladle, A., Steenweg, R., Shepherd, B. & Boyce, M. S. The role of human outdoor recreation in shaping patterns of grizzly bear-black bear co-occurrence. PLoS ONE 13, 1–16 (2018).Article 

    Google Scholar 
    Brooks, M. E. et al. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 9, 378–400 (2017).Article 

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

    Google Scholar 
    Agostinelli, C. & Lund, U. R package ‘circular’: circular statistics (version 0.4-94.1 (2022). https://r-forge.r-project.org/projects/circular/.Santos, F. et al. Prey availability and temporal partitioning modulate felid coexistence in Neotropical forests. PLoS ONE 14, 1–23 (2019).Article 

    Google Scholar 
    Olea, P. P., Iglesias, N. & Mateo-Tomás, P. Temporal resource partitioning mediates vertebrate coexistence at carcasses: the role of competitive and facilitative interactions. Basic Appl. Ecol. 60, 63–75 (2022).Article 

    Google Scholar 
    Shilling, F. et al. A reprieve from US wildlife mortality on roads during the COVID-19 pandemic. Biol. Conserv. 256, 109013 (2021).Article 

    Google Scholar 
    Behera, A. K. et al. The impacts of COVID-19 lockdown on wildlife in Deccan Plateau. India. Sci. Total Environ. 822, 153268 (2022).Article 
    ADS 
    CAS 

    Google Scholar 
    Procko, M., Naidoo, R., LeMay, V. & Burton, A. C. Human impacts on mammals in and around a protected area before, during, and after COVID-19 lockdowns. Conserv. Sci. Pract. 4, e12743. https://doi.org/10.1111/csp2.12743 (2022).Article 

    Google Scholar 
    Sanderfoot, O. V., Kaufman, J. D. & Gardner, B. Drivers of avian habitat use and detection of backyard birds in the Pacific Northwest during COVID-19 pandemic lockdowns. Sci. Rep. 12, 12655 (2022).Article 
    ADS 
    CAS 

    Google Scholar 
    Nevin, J. A. & Grace, R. C. Behavioral momentum and the law of effect. Behav. Brain Sci. 23, 73–90 (2000).Article 
    CAS 

    Google Scholar 
    Kautz, T. M. et al. Large carnivore response to human road use suggests a landscape of coexistence. Glob. Ecol. Conserv. 30, e01772 (2021).Article 

    Google Scholar 
    Frey, S., Volpe, J. P., Heim, N. A., Paczkowski, J. & Fisher, J. T. Move to nocturnality not a universal trend in carnivore species on disturbed landscapes. Oikos 129, 1128–1140 (2020).Article 

    Google Scholar 
    Schwartz, C. C. et al. Contrasting activity patterns of sympatric and allopatric black and grizzly bears. J. Wildl. Manag. 74, 1628–1638 (2010).Article 

    Google Scholar 
    Fortin, J. K. et al. Impacts of human recreation on brown bears (Ursus arctos): a review and new management tool. PLoS ONE 11, 1–26 (2016).Article 

    Google Scholar 
    Kendall, K. C. et al. Grizzly bear density in Glacier National Park. Montana. J. Wildl. Manag. 72, 1693–1705 (2008).Article 

    Google Scholar 
    Stetz, J. B., Kendall, K. C. & Macleod, A. C. Black bear density in Glacier National Park, Montana. Wildl. Soc. Bull. 38, 60–70 (2014).Article 

    Google Scholar 
    Sargeant, A. B. & Allen, S. H. Observed interactions between coyotes and red foxes. J. Mamm. 70, 631–633 (1989).Article 

    Google Scholar 
    Newsome, T. M. & Ripple, W. J. A continental scale trophic cascade from wolves through coyotes to foxes. J. Anim. Ecol. 84, 49–59 (2015).Article 

    Google Scholar 
    Naylor, L. M., Wisdom, M. J. & Anthony, R. G. Behavioral responses of North American elk to recreational activity. J. Wildl. Manag. 73, 328–338 (2009).Article 

    Google Scholar 
    Sarmento, W. M. & Berger, J. Human visitation limits the utility of protected areas as ecological baselines. Biol. Conserv. 212, 316–326 (2017).Article 

    Google Scholar 
    Garber, S. D. & Burger, J. A 20-year study documenting the relationship between turtle decline and human recreation. Ecol. Appl. 5, 1151–1162 (1995).Article 

    Google Scholar 
    Winter, P. L., Selin, S., Cerveny, L. & Bricker, K. Outdoor recreation, nature-based tourism, and sustainability. Sustainability 12, 1–12 (2020).
    Google Scholar 
    Geffroy, B., Samia, D. S. M., Bessa, E. & Blumstein, D. T. How nature-based tourism might increase prey vulnerability to predators. TREE 30, 755–765 (2015).
    Google Scholar 
    Eagles, P. F. J., McCool, S. F. & Haynes, C. D. Sustainable Tourism in Protected Areas: Guidelines for Planning and Management Vol. 8 (IUCN, 2002).Book 

    Google Scholar  More

  • in

    Gene loss and symbiont switching during adaptation to the deep sea in a globally distributed symbiosis

    Cavanaugh CM, McKiness ZP, Newton ILG, Stewart FJ. Marine chemosynthetic symbioses. Prokaryotes. 2006;1:475–507.Article 

    Google Scholar 
    Beinart RA, Luo C, Konstantinidis KT, Stewart FJ, Girguis PR. The bacterial symbionts of closely related hydrothermal vent snails with distinct geochemical habitats show broad similarity in chemoautotrophic gene content. Front Microbiol. 2019;10:1818.Article 

    Google Scholar 
    Robidart JC, Bench SR, Feldman RA, Novoradovsky A, Podell SB, Gaasterland T, et al. Metabolic versatility of the Riftia pachyptila endosymbiont revealed through metagenomics. Environ Microbiol. 2008;10:727–37.Article 
    CAS 

    Google Scholar 
    Ponnudurai R, Sayavedra L, Kleiner M, Heiden SE, Thürmer A, Felbeck H, et al. Genome sequence of the sulfur-oxidizing Bathymodiolus thermophilus gill endosymbiont. Stand Genom Sci. 2017;12:50.Article 

    Google Scholar 
    Duperron S, Bergin C, Zielinski F, Blazejak A, Pernthaler A, McKiness ZP, et al. A dual symbiosis shared by two mussel species, Bathymodiolus azoricus and Bathymodiolus puteoserpentis (Bivalvia: Mytilidae), from hydrothermal vents along the northern Mid-Atlantic Ridge. Environ Microbiol. 2006;8:1441–7.Article 
    CAS 

    Google Scholar 
    Dubilier N, Bergin C, Lott C. Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol. 2008;6:725–40.Article 
    CAS 

    Google Scholar 
    Sogin EM, Leisch N, Dubilier N. Chemosynthetic symbioses. Curr Biol. 2020;30:R1137–R1142.Article 
    CAS 

    Google Scholar 
    Roeselers G, Newton ILG. On the evolutionary ecology of symbioses between chemosynthetic bacteria and bivalves. Appl Microbiol Biotechnol. 2012;94:1–10.Article 
    CAS 

    Google Scholar 
    Moran NA. Symbiosis as an adaptive process and source of phenotypic complexity. Proc Natl Acad Sci USA. 2007;104 Suppl 1:8627–33.Article 
    CAS 

    Google Scholar 
    McMullen JG, Peterson BF, Forst S, Blair HG, Patricia Stock S. Fitness costs of symbiont switching using entomopathogenic nematodes as a model. BMC Evol Biol. 2017;17. https://doi.org/10.1186/s12862-017-0939-6.Taylor JD, Glover E. Biology, evolution and generic review of the chemosymbiotic bivalve family Lucinidae. London, UK: Ray Society; 2021.Osvatic JT, Wilkins LGE, Leibrecht L, Leray M, Zauner S, Polzin J, et al. Global biogeography of chemosynthetic symbionts reveals both localized and globally distributed symbiont groups. Proc Natl Acad Sci USA. 2021;118. https://doi.org/10.1073/pnas.2104378118.Petersen JM, Kemper A, Gruber-Vodicka H, Cardini U, van der Geest M, Kleiner M, et al. Chemosynthetic symbionts of marine invertebrate animals are capable of nitrogen fixation. Nat Microbiol. 2016;2:16195.Article 
    CAS 

    Google Scholar 
    Lim SJ, Davis B, Gill D, Swetenburg J, Anderson LC, Engel AS, et al. Gill microbiome structure and function in the chemosymbiotic coastal lucinid Stewartia floridana. FEMS Microbiol Ecol. 2021;97. https://doi.org/10.1093/femsec/fiab042.Lim SJ, Davis BG, Gill DE, Walton J, Nachman E, Engel AS, et al. Taxonomic and functional heterogeneity of the gill microbiome in a symbiotic coastal mangrove lucinid species. ISME J. 2019;13:902–20.Article 
    CAS 

    Google Scholar 
    Gros O, Liberge M, Felbeck H. Interspecific infection of aposymbiotic juveniles of Codakia orbicularis by various tropical lucinid gill-endosymbionts. Mar Biol. 2003;142:57–66.Article 

    Google Scholar 
    Gros O, Elisabeth NH, Gustave SDD, Caro A, Dubilier N. Plasticity of symbiont acquisition throughout the life cycle of the shallow-water tropical lucinid Codakia orbiculata (Mollusca: Bivalvia). Environ Microbiol. 2012;14:1584–95.Article 
    CAS 

    Google Scholar 
    Gros O, Frenkiel L, Mouëza M. Embryonic, larval, and post-larval development in the symbiotic clam Codakia orbicularis (Bivalvia: Lucinidae). Invertebr Biol. 1997;116:86–101.Article 

    Google Scholar 
    König S, Gros O, Heiden SE, Hinzke T, Thürmer A, Poehlein A, et al. Nitrogen fixation in a chemoautotrophic lucinid symbiosis. Nat Microbiol. 2016;2:16193.Article 

    Google Scholar 
    Fiore CL, Jarett JK, Olson ND, Lesser MP. Nitrogen fixation and nitrogen transformations in marine symbioses. Trends Microbiol. 2010;18:455–63.Article 
    CAS 

    Google Scholar 
    Cardini U, Bednarz VN, Foster RA, Wild C. Benthic N2 fixation in coral reefs and the potential effects of human-induced environmental change. Ecol Evol. 2014;4:1706–27.Article 

    Google Scholar 
    Glover EA, Taylor JD. Lucinidae of the Philippines: highest known diversity and ubiquity of chemosymbiotic bivalves from intertidal to bathyal depths (Mollusca: Bivalvia). mém Mus Natl Hist Nat. 2016;208:65–234.
    Google Scholar 
    Taylor JD, Glover EA, Williams ST. Diversification of chemosymbiotic bivalves: origins and relationships of deeper water Lucinidae. Biol J Linn Soc Lond. 2014;111:401–20.Article 

    Google Scholar 
    von Cosel R. Taxonomy of tropical West African bivalves. VI. Remarks on Lucinidae (Mollusca, Bivalvia), with description of six new genera and eight new species. Zoosystema. 2006;28:805.
    Google Scholar 
    Glover EA, Taylor JD, Rowden AA. Bathyaustriella thionipta, a new lucinid bivalve from a hydrothermal vent on the Kermadec Ridge, New Zealand and its relationship to shallow-water taxa (Bivalvia: Lucinidae). J Mollusca Stud. 2004;70:283–95.Article 

    Google Scholar 
    Paulus E Shedding light on deep-sea biodiversity—a highly vulnerable habitat in the face of anthropogenic change. Front Mar Sci. 2021;8. https://doi.org/10.3389/fmars.2021.667048.Brown A, Thatje S. Explaining bathymetric diversity patterns in marine benthic invertebrates and demersal fishes: physiological contributions to adaptation of life at depth. Biol Rev Camb Philos Soc. 2014;89:406–26.Article 

    Google Scholar 
    Smith CR, De Leo FC, Bernardino AF, Sweetman AK, Arbizu PM. Abyssal food limitation, ecosystem structure and climate change. Trends Ecol Evol. 2008;23:518–28.Article 

    Google Scholar 
    Gage JD, Tyler PA. Deep-sea biology: a natural history of organisms at the deep-sea floor. Cambridge, UK: Cambridge University Press; 1991.Iken K, Brey T, Wand U, Voigt J, Junghans P. Food web structure of the benthic community at the Porcupine Abyssal Plain (NE Atlantic): a stable isotope analysis. Prog Oceanogr. 2001;50:383–405.Article 

    Google Scholar 
    von Cosel R, Bouchet P. Tropical deep-water lucinids (Mollusca: Bivalvia) from the Indo-Pacific: essentially unknown, but diverse and occasionally gigantic. mém Mus Natl Hist Nat. 2008;196:115–213.
    Google Scholar 
    Stearns REC Scientific results of explorations by the US Fish Commission steamer Albatross. No. XVII. Descriptions of new West American land, fresh-water, and marine shells, with notes and comments. Proceedings of the United States National Museum. 1890. https://repository.si.edu/bitstream/handle/10088/13174/1/USNMP-13_813_1890.pdf.Taylor JD, Glover EA. The lucinid bivalve genus Cardiolucina (Mollusca, Bivalvia, Lucinidae): systematics, anatomy and relationships. Bull Br Mus Nat Hist Zoo. 1997;63:93–122.
    Google Scholar 
    Coan EV, Valentich-Scott P, Sadeghian PS. Bivalve seashells of tropical West America: marine bivalve mollusks from Baja California to Northern Peru. Santa Barbara, USA: Museum of Natural History; 2012.von Cosel R, Gofas S. Marine bivalves of tropical West Africa: from Rio de Oro to southern Angola. Marseille, France: Muséum national d’Histoire naturelle, Paris; 2019. p 1104.Atkinson L, Sink K. Field guide to the offshore marine invertebrates of South Africa. 2018. https://doi.org/10.15493/SAEON.PUB.10000001.Montagu G. Testacea Britannica, or natural history of British shells. London, UK: JS Hollis; 1803.Taylor J, Glover E. New lucinid bivalves from shallow and deeper water of the Indian and West Pacific Oceans (Mollusca, Bivalvia, Lucinidae). ZooKeys. 2013;326:69–90.Article 

    Google Scholar 
    Apprill A, McNally S, Parsons R, Weber L. Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquat Micro Ecol. 2015;75:129–37.Article 

    Google Scholar 
    Parada AE, Needham DM, Fuhrman JA. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol. 2016;18:1403–14.Article 
    CAS 

    Google Scholar 
    Pjevac P, Hausmann B, Schwarz J, Kohl G, Herbold CW, Loy A, et al. An economical and flexible dual barcoding, two-step PCR approach for highly multiplexed amplicon sequencing. Front Microbiol. 2021;12:669776.Article 

    Google Scholar 
    McLaren MR, Callahan BJ. Silva 138.1 prokaryotic SSU taxonomic training data formatted for DADA2 [Data set]. Zenodo. https://doi.org/10.5281/zenodo.4587955.Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–6.Article 
    CAS 

    Google Scholar 
    Andersen KS, Kirkegaard RH, Karst SM, Albertsen M. ampvis2: an R package to analyse and visualise 16S rRNA amplicon data. 2018. https://www.biorxiv.org/content/10.1101/299537v1.Bushnell B. BBMap: a fast, accurate, splice-aware aligner. Berkeley, CA, USA: Lawrence Berkeley National Lab. (LBNL); 2014.Nurk S, Meleshko D, Korobeynikov A, Pevzner PA. metaSPAdes: a new versatile metagenomic assembler. Genome Res. 2017;27:824–34.Article 
    CAS 

    Google Scholar 
    Nurk S, Bankevich A, Antipov D, Gurevich A, Korobeynikov A, Lapidus A, et al. Assembling genomes and mini-metagenomes from highly chimeric reads. In: Research in Computational Molecular Biology. Springer Berlin Heidelberg; 2013. p. 158–70.Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25:2078–9.Article 

    Google Scholar 
    Eren AM, Esen ÖC, Quince C, Vineis JH, Morrison HG, Sogin ML, et al. Anvi’o: an advanced analysis and visualization platform for ‘omics data. PeerJ. 2015;3:e1319.Article 

    Google Scholar 
    Alneberg J, Bjarnason BS, de Bruijn I, Schirmer M, Quick J, Ijaz UZ, et al. Binning metagenomic contigs by coverage and composition. Nat Methods. 2014;11:1144–6.Article 
    CAS 

    Google Scholar 
    Kang DD, Li F, Kirton E, Thomas A, Egan R, An H, et al. MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies. PeerJ. 2019;7:e7359.Article 

    Google Scholar 
    Olm MR, Brown CT, Brooks B, Banfield JF. dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication. ISME J. 2017;11:2864–8.Article 
    CAS 

    Google Scholar 
    Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25:1043–55.Article 
    CAS 

    Google Scholar 
    Chaumeil P-A, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics. 2019. https://doi.org/10.1093/bioinformatics/btz848.Parks DH, Chuvochina M, Chaumeil P-A, Rinke C, Mussig AJ, Hugenholtz P. A complete domain-to-species taxonomy for Bacteria and Archaea. Nat Biotechnol. 2020;38:1079–86.Article 
    CAS 

    Google Scholar 
    Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A, Chaumeil P-A, et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol. 2018;36:996–1004.Article 
    CAS 

    Google Scholar 
    Matsen FA, Kodner RB, Armbrust EV. pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree. BMC Bioinform. 2010;11:538.Article 

    Google Scholar 
    Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun. 2018;9:5114.Article 

    Google Scholar 
    Hyatt D, Chen G-L, Locascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinform. 2010;11:119.Article 

    Google Scholar 
    Price MN, Dehal PS, Arkin AP. FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS ONE. 2010;5:e9490.Article 

    Google Scholar 
    Eddy SR. Accelerated profile HMM searches. PLoS Comput Biol. 2011;7:e1002195.Article 
    CAS 

    Google Scholar 
    Ondov BD, Treangen TJ, Melsted P, Mallonee AB, Bergman NH, Koren S, et al. Mash: fast genome and metagenome distance estimation using MinHash. Genome Biol. 2016;17:132.Article 

    Google Scholar 
    Trifinopoulos J, Nguyen L-T, von Haeseler A, Minh BQ. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res. 2016;44:W232–5.Article 
    CAS 

    Google Scholar 
    Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 2021;49:W293–W296.Article 
    CAS 

    Google Scholar 
    Varghese NJ, Mukherjee S, Ivanova N, Konstantinidis KT, Mavrommatis K, Kyrpides NC, et al. Microbial species delineation using whole genome sequences. Nucleic Acids Res. 2015;43:6761–71.Article 
    CAS 

    Google Scholar 
    Qin Q-L, Xie B-B, Zhang X-Y, Chen X-L, Zhou B-C, Zhou J, et al. A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol. 2014;196:2210–5.Article 

    Google Scholar 
    Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund SK, Cook H, et al. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res. 2019;47:D309–D314.Article 
    CAS 

    Google Scholar 
    Huerta-Cepas J, Forslund K, Coelho LP, Szklarczyk D, Jensen LJ, von Mering C, et al. Fast genome-wide functional annotation through orthology assignment by eggNOG-Mapper. Mol Biol Evol. 2017;34:2115–22.Article 
    CAS 

    Google Scholar 
    Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S, Olsen GJ, et al. RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep. 2015;5:8365.Article 

    Google Scholar 
    Mahram A, Herbordt MC. NCBI BLASTP on high-performance reconfigurable computing systems. ACM Trans Reconfigurable Technol Syst. 2015;7:1–20.Article 

    Google Scholar 
    Yang Z. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci. 1997;13:555–6.CAS 

    Google Scholar 
    Osvatic J, Wilkins L. Strength of selection scripts. FigShare. 2022;8. https://doi.org/10.6084/m9.figshare.20626746.v1.Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol. 1990;56:1919–25.Article 
    CAS 

    Google Scholar 
    Lan Y, Sun J, Chen C, Sun Y, Zhou Y, Yang Y, et al. Hologenome analysis reveals dual symbiosis in the deep-sea hydrothermal vent snail Gigantopelta aegis. Nat Commun. 2021;12:1165.Article 
    CAS 

    Google Scholar 
    Leray M, Wilkins LGE, Apprill A, Bik HM, Clever F, Connolly SR, et al. Natural experiments and long-term monitoring are critical to understand and predict marine host-microbe ecology and evolution. PLoS Biol. 2021;19:e3001322.Article 
    CAS 

    Google Scholar 
    Petersen Jillian M, Yuen B, Alexandre G. The symbiotic ‘all-rounders’: partnerships between marine animals and chemosynthetic nitrogen-fixing bacteria. Appl Environ Microbiol 2020;87:e02129–20.Johnson KS, Childress JJ, Hessler RR, Sakamoto-Arnold CM, Beehler CL. Chemical and biological interactions in the Rose Garden hydrothermal vent field, Galapagos spreading center. Deep Sea Res A. 1988;35:1723–44.Article 

    Google Scholar 
    Kennicutt ME II, Brooks JM, Burke RA Jr. Hydrocarbon seepage, gas hydrates, and authigenic carbonate in the northwestern Gulf of Mexico. Offshore Technology Conference; 1989. https://doi.org/10.4043/5952-ms.Lilley MD, Butterfield DA, Olson EJ, Lupton JE, Macko SA, McDuff RE. Anomalous CH4 and NH4+ concentrations at an unsedimented mid-ocean-ridge hydrothermal system. Nature. 1993;364:45–47.Article 
    CAS 

    Google Scholar 
    Von Damm KL, Edmond JM, Measures CI, Grant B. Chemistry of submarine hydrothermal solutions at Guaymas Basin, Gulf of California. Geochim Cosmochim Acta. 1985;49:2221–37.Article 

    Google Scholar 
    Lee RW, Thuesen EV, Childress JJ. Ammonium and free amino acids as nitrogen sources for the chemoautotrophic symbiosis Solemya reidi Bernard (Bivalvia: Protobranchia). J Exp Mar Bio Ecol. 1992;158:75–91.Article 
    CAS 

    Google Scholar 
    Sanders JG, Beinart RA, Stewart FJ, Delong EF, Girguis PR. Metatranscriptomics reveal differences in in situ energy and nitrogen metabolism among hydrothermal vent snail symbionts. ISME J. 2013;7:1556–67.Article 
    CAS 

    Google Scholar 
    Touchette BW, Burkholder JM. Review of nitrogen and phosphorus metabolism in seagrasses. J Exp Mar Bio Ecol. 2000;250:133–67.Article 
    CAS 

    Google Scholar 
    Fourqurean JW, Zieman JC, Powell GVN. Relationships between porewater nutrients and seagrasses in a subtropical carbonate environment. Mar Biol. 1992;114:57–65.Article 
    CAS 

    Google Scholar 
    Williams SL. Experimental studies of Caribbean seagrass bed development. Ecol Monogr. 1990;60:449–69.Article 

    Google Scholar 
    Herbert RA. Nitrogen cycling in coastal marine ecosystems. FEMS Microbiol Rev. 1999;23:563–90.Article 
    CAS 

    Google Scholar 
    Risgaard-Petersen N, Dalsgaard T, Rysgaard S, Christensen PB, Borum J, McGlathery K, et al. Nitrogen balance of a temperate eelgrass Zostera marina bed. Mar Ecol Prog Ser. 1998;174:281–91.Article 
    CAS 

    Google Scholar 
    Bristow LA, Dalsgaard T, Tiano L, Mills DB, Bertagnolli AD, Wright JJ, et al. Ammonium and nitrite oxidation at nanomolar oxygen concentrations in oxygen minimum zone waters. Proc Natl Acad Sci USA. 2016;113:10601–6.Article 
    CAS 

    Google Scholar 
    Karthäuser C, Ahmerkamp S, Marchant HK, Bristow LA, Hauss H, Iversen MH, et al. Small sinking particles control anammox rates in the Peruvian oxygen minimum zone. Nat Commun. 2021;12:3235.Article 

    Google Scholar 
    Kuypers MMM, Lavik G, Woebken D, Schmid M, Fuchs BM, Amann R, et al. Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc Natl Acad Sci USA. 2005;102:6478–83.Article 
    CAS 

    Google Scholar 
    Johnson KS, Beehler CL, Sakamoto-Arnold CM, Childress JJ. In situ measurements of chemical distributions in a deep-sea hydrothermal vent field. Science. 1986;231:1139–41.Article 
    CAS 

    Google Scholar 
    Childress JJ, Girguis PR. The metabolic demands of endosymbiotic chemoautotrophic metabolism on host physiological capacities. J Exp Biol. 2011;214:312–25.Article 
    CAS 

    Google Scholar 
    Hentschel U, Hand S, Felbeck H. The contribution of nitrate respiration to the energy budget of the symbiont-containing clam Lucinoma aequizonata: a calorimetric study. J Exp Biol. 1996;199:427–33.Article 
    CAS 

    Google Scholar 
    Breusing C, Mitchell J, Delaney J, Sylva SP, Seewald JS, Girguis PR, et al. Physiological dynamics of chemosynthetic symbionts in hydrothermal vent snails. ISME J. 2020;14:2568–79.Article 
    CAS 

    Google Scholar 
    Amorim K, Loick-Wilde N, Yuen B, Osvatic JT, Wäge-Recchioni J, Hausmann B, et al. Chemoautotrophy, symbiosis and sedimented diatoms support high biomass of benthic molluscs in the Namibian shelf. Sci Rep. 2022;12:9731.Article 
    CAS 

    Google Scholar 
    Breusing C, Johnson SB, Tunnicliffe V, Clague DA, Vrijenhoek RC, Beinart RA. Allopatric and sympatric drivers of speciation in Alviniconcha hydrothermal vent snails. Mol Biol Evol. 2020;37:3469–84.Article 
    CAS 

    Google Scholar 
    Giovannoni SJ, Cameron Thrash J, Temperton B. Implications of streamlining theory for microbial ecology. ISME J. 2014;8:1553–65.Article 

    Google Scholar 
    Brissac T, Gros O, Merçot H. Lack of endosymbiont release by two Lucinidae (Bivalvia) of the genus Codakia: consequences for symbiotic relationships. FEMS Microbiol Ecol. 2009;67:261–7.Article 
    CAS 

    Google Scholar 
    Werner GDA, Cornelissen JHC, Cornwell WK, Soudzilovskaia NA, Kattge J, West SA, et al. Symbiont switching and alternative resource acquisition strategies drive mutualism breakdown. Proc Natl Acad Sci USA. 2018;115:5229–34.Article 
    CAS 

    Google Scholar 
    Sudakaran S, Kost C, Kaltenpoth M. Symbiont acquisition and replacement as a source of ecological innovation. Trends Microbiol. 2017;25:375–90.Article 
    CAS 

    Google Scholar 
    Li Y, Liles MR, Halanych KM. Endosymbiont genomes yield clues of tubeworm success. ISME J. 2018;12:2785–95.Article 
    CAS 

    Google Scholar 
    Moran NA, Yun Y. Experimental replacement of an obligate insect symbiont. Proc Natl Acad Sci USA. 2015;112:2093–6.Article 
    CAS 

    Google Scholar 
    Sørensen MES, Wood AJ, Cameron DD, Brockhurst MA. Rapid compensatory evolution can rescue low fitness symbioses following partner switching. Curr Biol. 2021;31:3721–3728.e4.Article 

    Google Scholar 
    Taylor JD, Glover EA, Smith L, Ikebe C, Williams ST. New molecular phylogeny of Lucinidae: increased taxon base with focus on tropical Western Atlantic species (Mollusca: Bivalvia). Zootaxa. 2016;4196:zootaxa.4196.3.2.Article 

    Google Scholar 
    Osvatic J. Fig1 gtdb tree and alignment. figshare. 2021. https://doi.org/10.6084/m9.figshare.16837216.v1.Osvatic J. Figure 2: GTDB alignment and phylogeny. 2021. https://doi.org/10.6084/m9.figshare.16837237. More

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    Investigating metropolitan change through mathematical morphology and a dynamic factor analysis of structural and functional land-use indicators

    Alphan, H. Land use change and urbanisation of Adana, Turkey. Land Degrad. Dev. 14, 575–586 (2003).Article 

    Google Scholar 
    Catalàn, B., Sauri, D. & Serra, P. Urban sprawl in the Mediterranean? Patterns of growth and change in the Barcelona Metropolitan Region 1993–2000. Landsc. Urban Plan. 85(3–4), 174–184 (2008).
    Google Scholar 
    Chen, K., Long, H., Liao, L., Tu, S. & Li, T. Land use transitions and urban-rural integrated development: Theoretical framework and China’s evidence. Land Use Policy 92, 104465 (2020).Article 

    Google Scholar 
    Bianchini, L. et al. Forest transition and metropolitan transformations in developed countries: Interpreting apparent and latent dynamics with local regression models. Land 11(1), 12 (2021).Article 

    Google Scholar 
    Angel, S., Parent, J., Civco, D. L., Blei, A. & Potere, D. The dimensions of global urban expansion: Estimates and projections for all countries, 2000–2050. Prog. Plan. 75(2), 53–107 (2011).Article 

    Google Scholar 
    Fischer, A. P. Forest landscapes as social-ecological systems and implications for management. Landsc. Urban Plan. 177, 138–147 (2018).Article 

    Google Scholar 
    Darvishi, A., Yousefi, M. & Marull, J. Modelling landscape ecological assessments of land use and cover change scenarios. Application to the Bojnourd Metropolitan Area (NE Iran). Land Use Policy 99, 105098 (2020).Article 

    Google Scholar 
    Cheng, L. L., Tian, C. & Yin, T. T. Identifying driving factors of urban land expansion using Google earth engine and machine-learning approaches in Mentougou District, China. Sci. Rep. 12(1), 1–13 (2022).Article 
    CAS 

    Google Scholar 
    Kasanko, M. et al. Are European Cities becoming dispersed? A comparative analysis of fifteen European urban areas. Landsc. Urban Plan. 77(1–2), 111–130 (2006).Article 

    Google Scholar 
    Terzi, F. & Bolen, F. Urban sprawl measurement of Istanbul. Eur. Plan. Stud. 17(10), 1559–1570 (2009).Article 

    Google Scholar 
    Angel, S., Parent, J. & Civco, D. L. Ten compactness properties of circles: measuring shape in geography. Can. Geogr. 54, 441–461 (2010).Article 

    Google Scholar 
    Salvati, L., Gemmiti, R. & Perini, L. Land degradation in Mediterranean urban areas: An unexplored link with planning?. Area 44(3), 317–325 (2012).Article 

    Google Scholar 
    Attorre, F., Bruno, M., Francesconi, F., Valenti, R. & Bruno, F. Landscape changes of Rome through tree-lined roads. Landsc. Urban Plan. 49, 115–128 (2000).Article 

    Google Scholar 
    Turok, I. & Mykhnenko, V. The trajectories of European cities, 1960–2005. Cities 24(3), 165–182 (2007).Article 

    Google Scholar 
    Ioannidis, C., Psaltis, C. & Potsiou, C. Towards a strategy for control of suburban informal buildings through automatic change detection. Comput. Environ. Urban Syst. 33, 64–74 (2009).Article 

    Google Scholar 
    Grekousis, G., Manetos, P. & Photis, Y. N. Modeling urban evolution using neural networks, fuzzy logic and GIS: The case of the athens metropolitan area. Cities 30, 193–203 (2013).Article 

    Google Scholar 
    Salvati, L. Towards a polycentric region? The socioeconomic trajectory of Rome, an ‘Eternally Mediterranean’ city. Tijdschr. Econ. Soc. Geogr. 105(3), 268–284 (2014).Article 

    Google Scholar 
    Chorianopoulos, I., Pagonis, T., Koukoulas, S. & Drymoniti, S. Planning, competitiveness and sprawl in the Mediterranean city: The case of Athens. Cities 27, 249–259 (2010).Article 

    Google Scholar 
    Munafò, M., Salvati, L. & Zitti, M. Estimating soil sealing rate at national level—Italy as a case study. Ecol. Ind. 26, 137–140 (2013).Article 

    Google Scholar 
    Morelli, V. G., Rontos, K. & Salvati, L. Between suburbanisation and re-urbanisation: Revisiting the urban life cycle in a Mediterranean compact city. Urban Res. Pract. 7(1), 74–88 (2014).Article 

    Google Scholar 
    Basem Ajjur, S. & Al-Ghamdi, S. G. Exploring urban growth–climate change–flood risk nexus in fast growing cities. Sci. Rep. 12, 12265 (2022).Article 
    ADS 

    Google Scholar 
    Li, H. & Wu, J. Use and misuse of landscape indices. Landsc. Ecol. 19, 389–399 (2004).Article 

    Google Scholar 
    Salvati, L. Agro-forest landscape and the ‘fringe’city: A multivariate assessment of land-use changes in a sprawling region and implications for planning. Sci. Total Environ. 490, 715–723 (2014).Article 
    ADS 
    CAS 

    Google Scholar 
    Sang, X. et al. Intensity and stationarity analysis of land use change based on CART algorithm. Sci. Rep. 9(1), 1–12 (2019).Article 
    ADS 
    CAS 

    Google Scholar 
    Ettehadi Osgouei, P., Sertel, E. & Kabadayı, M. E. Integrated usage of historical geospatial data and modern satellite images reveal long-term land use/cover changes in Bursa/Turkey, 1858–2020. Sci. Rep. 12(1), 1–17 (2022).Article 

    Google Scholar 
    He, S., Yu, S., Li, G. & Zhang, J. Exploring the influence of urban form on land-use efficiency from a spatiotemporal heterogeneity perspective: Evidence from 336 Chinese cities. Land Use Policy 95, 104576 (2020).Article 

    Google Scholar 
    Bockarjova, M., Wouter Botzen, W. J., Bulkeley, H. A. & Toxopeus, H. Estimating the social value of nature-based solutions in European cities. Sci. Rep. 12, 19833 (2022).Article 
    ADS 
    CAS 

    Google Scholar 
    Liu, J. & Niyogi, D. Meta-analysis of urbanisation impact on rainfall modification. Sci. Rep. 9(1), 1–14 (2019).ADS 

    Google Scholar 
    Holland, J. H. Studying complex adaptive systems. J. Syst. Sci. Complex. 19(1), 1–8 (2006).Article 
    MathSciNet 
    MATH 

    Google Scholar 
    Salvati, L. & Serra, P. Estimating rapidity of change in complex urban systems: A multidimensional, local-scale approach. Geogr. Anal. 48(2), 132–156 (2016).Article 

    Google Scholar 
    Bura, S., Guerin-Pace, F., Mathian, H., Pumain, D. & Sanders, L. Multi-agents systems and the dynamics of a settlement system. Geogr. Anal. 28(2), 161–178 (1996).Article 

    Google Scholar 
    Hasse, J. E. & Lathrop, R. G. Land resource impact indicators of urban sprawl. Appl. Geogr. 23, 159–175 (2003).Article 

    Google Scholar 
    Grafius, D. R., Corstanje, R. & Harris, J. A. Linking ecosystem services, urban form and green space configuration using multivariate landscape metric analysis. Landsc. Ecol. 33(4), 557–573 (2018).Article 

    Google Scholar 
    Pumain, D. Hierarchy in Natural and Social Sciences (Kluwer-Springer, 2005).
    Google Scholar 
    Cabral, P., Augusto, G., Tewolde, M. & Araya, Y. Entropy in urban systems. Entropy 15(12), 5223–5236 (2013).Article 
    ADS 

    Google Scholar 
    Salvati, L. & Carlucci, M. In-between stability and subtle changes: Urban growth, population structure, and the city life cycle in Rome. Popul. Space Place 22(3), 216–227 (2016).Article 

    Google Scholar 
    Batty, M. & Longley, P. Fractal Cities (Academic Press, 1994).MATH 

    Google Scholar 
    Berry, B. J. L. Cities as systems within systems of cities. Pap. Reg. Sci. 13, 147–163 (2005).Article 

    Google Scholar 
    Petrosillo, I. et al. The resilient recurrent behavior of mediterranean semi-arid complex adaptive landscapes. Land 10(3), 296 (2021).Article 

    Google Scholar 
    Portugali, J. Complexity, Cognition and the City, Understanding Complex Systems (Springer, 2011).Book 

    Google Scholar 
    Wu, J., Jenerette, G. D., Buyantuyev, A. & Redman, C. L. Quantifying spatiotemporal patterns of urbanisation: The case of the two fastest growing metropolitan regions in the United States. Ecol. Complex. 8(1), 1–8 (2011).Article 

    Google Scholar 
    Sun, Y., Gao, C., Li, J., Li, W. & Ma, R. Examining urban thermal environment dynamics and relations to biophysical composition and configuration and socioeconomic factors: A case study of the Shanghai metropolitan region. Sustain. Cities Soc. 40, 284–295 (2018).Article 

    Google Scholar 
    Phillips, M. A. & Ritala, P. A complex adaptive systems agenda for ecosystem research methodology. Technol. Forecast. Soc. Change 148, 119739 (2019).Article 

    Google Scholar 
    Walker, B., Holling, C. S., Carpenter, S. R. & Kinzig, A. Resilience, adaptability and transformability in social-ecological systems. Ecol. Soc. 9(2), 5 (2004).Article 

    Google Scholar 
    Kelly, C. et al. Community resilience and land degradation in forest and shrublandsocio-ecological systems: A case study in Gorgoglione, Basilicata regionn, Italy. Land Use Policy 46, 11–20 (2015).Article 

    Google Scholar 
    Preiser, R., Biggs, R., De Vos, A. & Folke, C. Social-ecological systems as complex adaptive systems. Ecol. Soc. 23(4), 46 (2018).Article 

    Google Scholar 
    Ferrara, A. et al. Shaping the role of ‘fast’ and ‘slow’ drivers of change in forest-shrubland socio-ecological systems. J. Environ. Manag. 169, 155–166 (2016).Article 

    Google Scholar 
    Lamy, T., Liss, K. N., Gonzalez, A. & Bennett, E. M. Landscape structure affects the provision of multiple ecosystem services. Environ. Res. Lett. 11(12), 124017 (2016).Article 
    ADS 

    Google Scholar 
    Riitters, K. H., Vogt, P., Soille, P., Kozak, J. & Estreguil, C. Neutral model analysis of landscape patterns from mathematical morphology. Landsc. Ecol. 22(7), 1033–1043 (2007).Article 

    Google Scholar 
    Riitters, K., Vogt, P., Soille, P. & Estreguil, C. Landscape patterns from mathematical morphology on maps with contagion. Landsc. Ecol. 24(5), 699–709 (2009).Article 

    Google Scholar 
    Anas, A., Arnott, R. & Small, K. Urban spatial structure. J. Econ. Lit. 36(3), 1426–1464 (1998).
    Google Scholar 
    Arroyo-Mora, J. P., Sánchez-Azofeifa, G. A., Rivard, B., Calvo, J. C. & Janzen, D. H. Dynamics in landscape structure and composition for the Chorotega region, Costa Rica from 1960 to 2000. Agr. Ecosyst. Environ. 106(1), 27–39 (2005).Article 

    Google Scholar 
    Siles, G., Charland, A., Voirin, Y. & Bénié, G. B. Integration of landscape and structure indicators into a web-based geoinformation system for assessing wetlands status. Eco. Inform. 52, 166–176 (2019).Article 

    Google Scholar 
    Soille, P. Morphological Image Analysis: Principles and Applications (Springer, 2003).MATH 

    Google Scholar 
    Soille, P. & Vogt, P. Morphological segmentation of binary patterns. Pattern Recogn. Lett. 30, 456–459 (2009).Article 
    ADS 

    Google Scholar 
    Vogt, P. et al. Mapping spatial patterns with morphological image processing. Landsc. Ecol. 22(2), 171–177 (2007).Article 

    Google Scholar 
    Bajocco, S., Ceccarelli, T., Smiraglia, D., Salvati, L. & Ricotta, C. Modeling the ecological niche of long-term land use changes: The role of biophysical factors. Ecol. Ind. 60, 231–236 (2016).Article 

    Google Scholar 
    Yin, Y., Zhou, K. & Chen, Y. Deconstructing the driving factors of land development intensity from multi-scale in differentiated functional zones. Sci. Rep. 12(1), 1–13 (2022).Article 

    Google Scholar 
    Duvernoy, I., Zambon, I., Sateriano, A. & Salvati, L. Pictures from the other side of the fringe: Urban growth and peri-urban agriculture in a post-industrial city (Toulouse, France). J. Rural. Stud. 57, 25–35 (2018).Article 

    Google Scholar 
    Smiraglia, D., Ceccarelli, T., Bajocco, S., Salvati, L. & Perini, L. Linking trajectories of land change, land degradation processes and ecosystem services. Environ. Res. 147, 590–600 (2016).Article 
    CAS 

    Google Scholar 
    Shaker, R. R. Examining sustainable landscape function across the Republic of Moldova. Habitat Int. 72, 77–91 (2018).Article 
    ADS 

    Google Scholar 
    Zheng, H. & Li, H. Spatial–temporal evolution characteristics of land use and habitat quality in Shandong Province, China. Sci. Rep. 12(1), 1–12 (2022).Article 

    Google Scholar 
    Tombolini, I., Munafò, M. & Salvati, L. Soil sealing footprint as an indicator of dispersed urban growth: A multivariate statistics approach. Urban Res. Pract. 9(1), 1–15 (2016).Article 

    Google Scholar 
    Salvati, L., Sateriano, A., Grigoriadis, E. & Carlucci, M. New wine in old bottles: The (changing) socioeconomic attributes of sprawl during building boom and stagnation. Ecol. Econ. 131, 361–372 (2017).Article 

    Google Scholar 
    Zambon, I., Benedetti, A., Ferrara, C. & Salvati, L. Soil matters? A multivariate analysis of socioeconomic constraints to urban expansion in Mediterranean Europe. Ecol. Econ. 146, 173–183 (2018).Article 

    Google Scholar 
    Paul, V. & Tonts, M. Containing urban sprawl: Trends in land use and spatial planning in the Metropolitan Region of Barcelona. J. Environ. Plann. Manag. 48(1), 7–35 (2005).Article 

    Google Scholar 
    Serra, P., Vera, A., Tulla, A. F. & Salvati, L. Beyond urban–rural dichotomy: Exploring socioeconomic and land-use processes of change in Spain (1991–2011). Appl. Geogr. 55, 71–81 (2014).Article 

    Google Scholar 
    Seifollahi-Aghmiuni, S., Kalantari, Z., Egidi, G., Gaburova, L. & Salvati, L. Urbanisation-driven land degradation and socioeconomic challenges in peri-urban areas: Insights from Southern Europe. Ambio 51(6), 1446–1458 (2022).Article 

    Google Scholar 
    Pili, S., Grigoriadis, E., Carlucci, M., Clemente, M. & Salvati, L. Towards sustainable growth? A multi-criteria assessment of (changing) urban forms. Ecol. Ind. 76, 71–80 (2017).Article 

    Google Scholar 
    Salvati, L., Sateriano, A. & Grigoriadis, E. Crisis and the city: Profiling urban growth under economic expansion and stagnation. Lett. Spat. Resour. Sci. 9(3), 329–342 (2016).Article 

    Google Scholar 
    Champion, T. & Hugo, G. New Forms of Urbanisation: Beyond the Urban-Rural Dichotomy (Ashgate, 2004).
    Google Scholar 
    Frondoni, R., Mollo, B. & Capotorti, G. A landscape analysis of land cover change in the municipality of Rome (Italy): Spatio-temporal characteristics and ecological implications of land cover transitions from 1954 to 2001. Landsc. Urban Plan. 100(1–2), 117–128 (2011).Article 

    Google Scholar 
    Perrin, C., Nougarèdes, B., Sini, L., Branduini, P. & Salvati, L. Governance changes in peri-urban farmland protection following decentralisation: A comparison between Montpellier (France) and Rome (Italy). Land Use Policy 70, 535–546 (2018).Article 

    Google Scholar 
    Salvati, L. Monitoring high-quality soil consumption driven by urban pressure in a growing city (Rome, Italy). Cities 31, 349–356 (2013).Article 

    Google Scholar 
    Salvati, L., Ciommi, M. T., Serra, P. & Chelli, F. M. Exploring the spatial structure of housing prices under economic expansion and stagnation: The role of socio-demographic factors in metropolitan Rome, Italy. Land Use Policy 81, 143–152 (2019).Article 

    Google Scholar 
    Ferrara, C., Salvati, L. & Tombolini, I. An integrated evaluation of soil resource depletion from diachronic settlement maps and soil cartography in peri-urban Rome, Italy. Geoderma 232, 394–405 (2014).Article 
    ADS 

    Google Scholar 
    Egidi, G. & Salvati, L. Beyond the suburban-urban divide: Convergence in age structures in metropolitan Rome, Italy. J. Popul. Soc. Stud. 28(2), 130–142 (2020).Article 

    Google Scholar 
    Pili, S., Serra, P. & Salvati, L. Landscape and the city: Agro-forest systems, land fragmentation and the ecological network in Rome, Italy. Urban For. Urban Green. 41, 230–237 (2019).Article 

    Google Scholar 
    European Environment Agency. Urban Sprawl in Europe – The Ignored Challenge. Copenhagen: EEA Report no. 10 (2006).Park, S., Hepcan, Ç. C., Hepcan, Ş & Cook, E. A. Influence of urban form on landscape pattern and connectivity in metropolitan regions: a comparative case study of Phoenix, AZ, USA, and Izmir, Turkey. Environ. Monit. Assess. 186(10), 6301–6318 (2014).Article 

    Google Scholar 
    Luo, F., Liu, Y., Peng, J. & Wu, J. Assessing urban landscape ecological risk through an adaptive cycle framework. Landsc. Urban Plan. 180, 125–134 (2018).Article 

    Google Scholar 
    Ortega, M., Pascual, S., Elena-Rosselló, R. & Rescia, A. J. Land-use and spatial resilience changes in the Spanish olive socio-ecological landscape. Appl. Geogr. 117, 102171 (2020).Article 

    Google Scholar 
    Parcerisas, L. et al. Land use changes, landscape ecology and their socioeconomic driving forces in the Spanish Mediterranean coast (El Maresme County, 1850–2005). Environ. Sci. Policy 23, 120–132 (2012).Article 

    Google Scholar 
    Masini, E. et al. Urban growth, land-use efficiency and local socioeconomic context: A comparative analysis of 417 metropolitan regions in Europe. Environ. Manag. 63(3), 322–337 (2019).Article 
    ADS 

    Google Scholar 
    Luck, M. & Wu, J. A gradient analysis of urban landscape pattern: a case study from the Phoenix metropolitan region, Arizona, USA. Landsc. Ecol. 17(4), 327–339 (2002).Article 

    Google Scholar 
    Pesaresi, M. & Bianchin, A. Recognising settlement structure using mathematical morphology and image texture. Remote Sensing Urban Anal. GISDATA 9, 46–60 (2003).
    Google Scholar 
    Schneider, A. & Woodcock, C. E. Compact, dispersed, fragmented, extensive? A comparison of urban growth in twenty-five global cities using remotely sensed data, pattern metrics and census information. Urban Stud. 45(3), 659–692 (2008).Article 

    Google Scholar 
    Mubareka, S., Koomen, E., Estreguil, C. & Lavalle, C. Development of a composite index of urban compactness for land use modelling applications. Landsc. Urban Plan. 103(3–4), 303–317 (2011).Article 

    Google Scholar 
    Vogt, P. et al. Mapping landscape corridors. Ecol. Ind. 7(2), 481–488 (2007).Article 

    Google Scholar 
    Daya Sagar, B. S. & Murthy, K. S. R. Generation of a fractal landscape using nonlinear mathematical morphological transformations. Fractals 8(03), 267–272 (2000).Article 

    Google Scholar 
    Scott, A. J., Carter, C., Reed, M. R., Stonyer, B. & Coles, R. Disintegrated development at the rural-urban fringe: Re-connecting spatial planning theory and practice. Prog. Plan. 83, 1–52 (2013).Article 

    Google Scholar 
    Zhao, Q., Wen, Z., Chen, S., Ding, S. & Zhang, M. Quantifying land use/land cover and landscape pattern changes and impacts on ecosystem services. Int. J. Environ. Res. Public Health 17(1), 126 (2020).Article 

    Google Scholar 
    Parr, J. The regional economy, spatial structure and regional urban systems. Reg. Stud. 48(12), 1926–1938 (2014).Article 

    Google Scholar 
    Salvati, L., Zambon, I., Chelli, F. M. & Serra, P. Do spatial patterns of urbanisation and land consumption reflect different socioeconomic contexts in Europe?. Sci. Total Environ. 625, 722–730 (2018).Article 
    ADS 
    CAS 

    Google Scholar 
    Coppi, R. & Bolasco, S. Multiway Data Analysis (Elsevier, 1988).MATH 

    Google Scholar 
    Kroonenberg, P. M. Applied Multiway Data Analysis (Wiley, 2008).Book 
    MATH 

    Google Scholar 
    Escofier, B. & Pages, J. Multiple factor analysis (AFMULT Package). Comput. Stat. Data Anal. 18, 121–140 (1994).Article 
    MATH 

    Google Scholar 
    De Rosa, S. & Salvati, L. Beyond a ‘side street story’? Naples from spontaneous centrality to entropic polycentricism, towards a ‘crisis city’. Cities 51, 74–83 (2016).Article 

    Google Scholar 
    Favaro, J.-M. & Pumain, D. Gibrat revisited: An urban growth model incorporating spatial interaction and innovation cycles. Geogr. Anal. 43(3), 261–286 (2011).Article 

    Google Scholar 
    Walker, B. H., Carpenter, S. R., Rockstrom, J., Crepin, A.-S. & Peterson, G. D. “Drivers, “slow” variables, “fast” variables, shocks, and resilience. Ecol. Soc. 17(3), 30 (2012).Article 

    Google Scholar 
    Zhang, Z., Su, S., Xiao, R., Jiang, D. & Wu, J. Identifying determinants of urban growth from a multi-scale perspective: A case study of the urban agglomeration around Hangzhou Bay, China. Appl. Geogr. 45, 193–202 (2013).Article 

    Google Scholar 
    Fratarcangeli, C., Fanelli, G., Franceschini, S., De Sanctis, M. & Travaglini, A. Beyond the urban-rural gradient: Self-organising map detects the nine landscape types of the city of Rome. Urban For. Urban Green. 38, 354–370 (2019).Article 

    Google Scholar 
    Crisci, M., Benassi, F., Rabiei-Dastjerdi, H., McArdle, G. Spatio-temporal variations and contextual factors of the supply of Airbnb in Rome. An initial investigation. Lett. Spat. Resour. Sci. 1–17 (2022).Lelo, K., Monni, S. & Tomassi, F. Socio-spatial inequalities and urban transformation. The case of Rome districts. Socio-Econ. Plann. Sci. 68, 100696 (2019).Article 

    Google Scholar 
    Crisci, M. The impact of the real estate crisis on a south european metropolis: From urban diffusion to Reurbanisation. Appl. Spat. Anal. Policy 15(3), 797–820 (2022).Article 

    Google Scholar 
    Wang, Y. & Zhang, X. A dynamic modeling approach to simulating socioeconomic effects on landscape changes. Ecol. Model. 140(1–2), 141–162 (2001).Article 

    Google Scholar 
    Voghera, A. The River agreement in Italy. Resilient planning for the co-evolution of communities and landscapes. Land Use Policy 91, 104377 (2020).Article 

    Google Scholar 
    Chen, A. & Partridge, M. D. When are cities engines of growth in China? Spread and backwash effects across the urban hierarchy. Reg. Stud. 47(8), 1313–1331 (2013).Article 

    Google Scholar 
    Ciommi, M., Chelli, F. M., Carlucci, M. & Salvati, L. Urban growth and demographic dynamics in southern Europe: Toward a new statistical approach to regional science. Sustainability 10(8), 2765 (2018).Article 

    Google Scholar 
    Jacobs-Crisioni, C., Rietveld, P. & Koomen, E. The impact of spatial aggregation on urban development analyses. Appl. Geogr. 47, 46–56 (2014).Article 

    Google Scholar 
    Kourtit, K., Nijkamp, P. & Reid, N. The new urban world: Challenges and policy. Appl. Geogr. 49, 1–3 (2014).Article 

    Google Scholar 
    Bruegmann, R. Sprawl: A Compact History (University of Chicago Press, 2005).Book 

    Google Scholar 
    Neuman, M. & Hull, A. The Futures of the City Region. Reg. Stud. 43(6), 777–787 (2009).Article 

    Google Scholar 
    Couch, C., Petschel-held, G. & Leontidou, L. Urban Sprawl In Europe: Landscapes, Land-use Change and Policy (Blackwell, 2007).Book 

    Google Scholar 
    Longhi, C. & Musolesi, A. European cities in the process of economic integration: towards structural convergence. Ann. Reg. Sci. 41, 333–351 (2007).Article 

    Google Scholar 
    Tian, G., Ouyang, Y., Quan, Q. & Wu, J. Simulating spatiotemporal dynamics of urbanisation with multi-agent systems—A case study of the Phoenix metropolitan region, USA. Ecol. Model. 222(5), 1129–1138 (2011).Article 

    Google Scholar 
    Tian, L., Chen, J. & Yu, S. X. Coupled dynamics of urban landscape pattern and socioeconomic drivers in Shenzhen, China. Landsc. Ecol. 29(4), 715–727 (2014).Article 

    Google Scholar 
    Fielding, A. J. Counterurbanization in Western Europe. Prog. Plan. 17, 1–52 (1982).Article 

    Google Scholar 
    Oueslati, W., Alvanides, S. & Garrod, G. Determinants of urban sprawl in European cities. Urban Stud. 52(9), 1594–1614 (2015).Article 

    Google Scholar 
    Tress, B., Tress, G., Décamps, H. & d’Hauteserre, A. M. Bridging human and natural sciences in landscape research. Landsc. Urban Plan. 57(3–4), 137–141 (2001).Article 

    Google Scholar 
    Xu, Z., Lv, Z., Li, J., Sun, H. & Sheng, Z. A Novel perspective on travel demand prediction considering natural environmental and socioeconomic factors. IEEE Intell. Transp. Syst. Mag. https://doi.org/10.1109/MITS.2022.3162901 (2022).Article 

    Google Scholar 
    Xu, Z., Lv, Z., Li, J. & Shi, A. A novel approach for predicting water demand with complex patterns based on ensemble learning. Water Resour. Manag. 36(11), 4293–4312 (2022).Article 

    Google Scholar 
    Lv, Z., Li, J., Dong, C., Li, H. & Xu, Z. Deep learning in the COVID-19 epidemic: A deep model for urban traffic revitalisation index. Data Knowl. Eng. 135, 101912 (2021).Article 

    Google Scholar  More

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    Altered gut microbiota in individuals with episodic and chronic migraine

    ParticipantsIn total, 80, 63, and 56 participants in the EM, CM, and control groups, respectively, initially agreed to participate in this study. Nevertheless, 28, 12, and 13 individuals in the EM, CM, and control groups, respectively, withdrew their participation and did not bring any fecal samples to the study site. After providing fecal samples, 10 and 6 individuals with EM and CM, respectively, reported intake of probiotics and were excluded from the analysis. No participant in the control group consumed probiotics during the study period. Eventually, 42, 45, and 43 participants in the EM, CM, and control groups, respectively, were enrolled (Fig. 1). The demographic and clinical characteristics of participants are summarized in Table 1. All participants with EM and CM used acute treatments for migraine. Moreover, 25 (59.5%) and 27 (60.0%) participants with EM and CM, respectively, received prophylactic treatment for migraine. Of the 42 participants with EM, 20 used anti-epileptic medications, 11 used beta blockers, 2 used an anti-depressant, and 1 used a calcium-channel blocker for prophylactic treatment. Of the 45 participants with CM, 23 used anti-epileptic medications, 8 used beta blockers, 1 used an anti-depressant, and no participant used calcium-channel blockers for prophylactic treatment. No participant in the EM, CM, and control groups was infected with SARS-CoV-2 before or during participation in the study.Figure 1Flow of participants in a study on the composition of gut microbiota in participants with episodic or chronic migraine.Full size imageTable 1 Demographic and clinical characteristics of participants with episodic and chronic migraine and the control.Full size tableCollection of 16 s RNA sequencing dataWe obtained 7,802,425 read sequences, accounting for 99.8% of the valid sequences from the fecal samples of 130 participants. According to barcode and primer sequence filtering, an average of 59,305 (range, 3716–90,832) observed sequences per sample was recovered for downstream analysis. Thus, 2,242,325 sequences were obtained from the controls for phylogenetic analysis, whereas 2,747,952 and 2,812,148 sequences were obtained from the EM and CM groups, respectively.Microbial diversityAlpha diversity was defined as microbial community richness and evenness. Alpha diversities in the genus richness, as evaluated by Chao1 (Fig. 2A), Shannon (Fig. 2B), and Simpson (Fig. 2C) indices, did not differ significantly among the EM, CM, and control groups. Beta diversity represented the community composition dissimilarity between samples. PCoA with the weighted UniFrac distance (Fig. 3A and Supplementary Fig. S1A, p = 0.176, permutational multivariate analysis of variance [PERMANOVA]), the unweighted UniFrac distance (Fig. 3B and Supplementary Fig. S1B, p = 0.132, PERMANOVA), and the Bray–Curtis dissimilarity index (Fig. 3C and Supplementary Fig. S1C, p = 0.220, PERMANOVA) for beta diversity at the genus level among the EM, CM, and control groups revealed that these three groups could not be separated.Figure 2Alpha diversity at the genus level using Chao1 (A), Shannon (B), and Simpson (C) indices*,†. *Controls (green) and participants with episodic migraine (blue) and chronic migraine (yellow). †In the box plots, the lower boundary of the box indicates the 25th percentile; a blue line within the box marks the median, and the upper boundary of the box indicates the 75th percentile. Whiskers above (red) and below the box (green) indicate the highest and the lowest values, respectively.Full size imageFigure 3Beta diversity of microbiota in principal coordinate analysis plot with the weighted UniFrac distance (A), the unweighted UniFrac distance (B) and the Bray–Curtis dissimilarity index (C)*. *Controls (green) and participants with episodic migraine (blue) and chronic migraine (yellow).Full size imageRelative abundance of fecal microbes between participants with EM and the controlRelative abundance of fecal microbes at the phylum level did not differ significantly among participants in the control, EM, and CM groups (Supplementary Fig. S2). Moreover, Tissierellales (p = 0.001) and Tissierellia (p = 0.001) were more abundant in the EM group than that in the control group at the order and class levels, respectively (Fig. 4A). At the family level, Peptoniphilaceae (p = 0.001) and Eubacteriaceae (p = 0.045) occurred at a significantly higher proportion in the EM group than that in the control group. Furthermore, at the genus level, the abundance of 11 genera differed significantly between the two groups, including one more abundant and 10 less abundant genera in the EM group. Catenibacterium (p = 0.031) and Olsenella (p = 0.038) had the highest relative abundance in the control and EM groups, respectively.Figure 4Taxonomic differences in fecal microbiota among participants. The fold change (log2) denotes the difference in relative abundance between participants with episodic migraine and the control (A), between those with chronic migraine and the control (B), and between those with episodic and chronic migraine (C). CM chronic migraine; EM episodic migraine.Full size imageRelative abundance of fecal microbes between participants with CM and the controlThe analysis results at the class, order, family, genus, and species levels between CM and control groups are illustrated in Fig. 4B. Tissierellia (p = 0.001), Tissierellales (p = 0.001), and Peptoniphilaceae (p = 0.001) were more abundant in the CM group than that in the control group at the class, order, and family levels, respectively; however, at the genus level, the abundances of 18 genera differed significantly, including four more abundant and 14 less abundant genera in the CM group than in the control group.Relative abundance of fecal microbes between participants with EM and CMThe analysis results at the class, order, family, and genus levels between CM and EM groups are summarized in Fig. 4C. At the class level, Bacilli (p = 0.033) were less abundant in the CM group than that in the EM group; however, at the order level, Selenomonadales (p = 0.016) and Lactobacillales (p = 0.034) were less abundant in the CM group than that in the EM group. Moreover, at the class level, Selenomonadaceae (p = 0.016) and Prevotellaceae (p = 0.012) were less abundant in the CM group than that in the EM group. Furthermore, at the genus level, PAC001212_g (p = 0.019) revealed relative positive predominancy in the CM groups, whereas Prevotella (p = 0.019), Holdemanella (p = 0.009), Olsenella (p = 0.033), Adlercreutzia (p = 0.018), and Coprococcus (p = 0.040) revealed relative positive predominancy in the EM group.Association among fecal microbiota and clinical characteristics and comorbidities of migraineAmong the five genera (Roseburia, Eubacterium_g4, Agathobacter, PAC000195_g, and Catenibacterium) depicting predominance or less-predominance both in EM and CM groups, we conducted additional analyses for clinical characteristics and migraine comorbidities.Combining the results of the 42 and 45 participants with EM and CM, respectively, the Poisson regression analysis for relative abundance of microbiota revealed that a higher composition of PAC000195_g (p = 0.040) was significantly associated with lower headache frequency (Table 2). Furthermore, Agathobacter (p = 0.009) had a negative association with severe headache intensity (Table 3). Anxiety was associated with Catenibacterium (p = 0.027); however, depression did not reveal any association with the five genera (Table 3).Table 2 The association between headache frequency and the relative abundance of microbiota.*Full size tableTable 3 The association of severe headache intensity and comorbidities with the relative abundance of microbiota*.Full size tableRelative abundance of fecal microbes in participants with EM based on prophylactic treatmentAlpha and beta diversities in participants with EM did not differ significantly based on their prophylactic treatment (Supplementary Figs S3A–C, S4A–C, and S5A–C). At the genus level, Klebsiella (p = 0.009), Enterobacteriaceae_g (p = 0.006), and Faecalibacterium (p = 0.046) were more abundant in the prophylactic group than the non-prophylactic group (Supplementary Fig. S6A).Relative abundance of fecal microbes in participants with CM based on prophylactic treatmentAlpha and beta diversities in participants with CM did not differ significantly based on prophylactic treatment (Supplementary Figs S7A–C, S8A–C, and S9A–C). Emergencia (p = 0.043), Ruthenibacterium (p = 0.005), Eggerthella (p = 0.003), PAC000743_g (p = 0.034), and Anaerostipes (p = 0.039) were more abundant in the prophylactic group, whereas PAC000196_g (p = 0.049), Fusicatenibacter (p = 0.028), and Faecalibacterium (p = 0.021) were more abundant in the non-prophylactic group at the genus level (Supplementary Fig. S6B). More

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    Warmth shifts symbionts

    Abigail Meyer from the University of Minnesota, USA, and colleagues from the USA, investigated the physiological and morphological responses to experimental warming and CO2 additions in the widespread forest lichen Evernia mesomorpha. While impacts of CO2 were largely negligible, warming and associated drying was linked to decreases in biomass, carbon assimilation and respiration rates. As well as bleaching of the lichen, indicative of death of the photobiont, the authors found evidence of shifts in internal algal communities, including increased proportions of certain algal clades under warming. While the study reveals the sensitivity of lichen algae to warming, further work is needed to reveal whether photobiont turnover may assist in lichen acclimation and recovery. More