More stories

  • in

    The skilled ecosystem engineers with big teeth and paddle tails

    Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain
    the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in
    Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles
    and JavaScript. More

  • in

    Experimental transmission of Stony Coral Tissue Loss Disease results in differential microbial responses within coral mucus and tissue

    Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR, Grimes DJ, et al. Emerging marine diseases-climate links and anthropogenic factors. Science. 1999;285:1505–10. http://science.sciencemag.org/content/285/5433/1505.abstract.CAS 
    Article 

    Google Scholar 
    Maynard J, Van Hooidonk R, Eakin CM, Puotinen M, Garren M, Williams G, et al. Projections of climate conditions that increase coral disease susceptibility and pathogen abundance and virulence. Nat Clim Chang. 2015;5:688–94.Article 

    Google Scholar 
    Burge CA, Mark Eakin C, Friedman CS, Froelich B, Hershberger PK, Hofmann EE, et al. Climate change influences on marine infectious diseases: implications for management and society. Ann Rev Mar Sci. 2014;6:249–77.Article 

    Google Scholar 
    Miller J, Muller E, Rogers C, Waara R, Atkinson A, Whelan KRT, et al. Coral disease following massive bleaching in 2005 causes 60% decline in coral cover on reefs in the US Virgin Islands. Coral Reefs. 2009;28:925–37.Article 

    Google Scholar 
    Walton CJ, Hayes NK, Gilliam DS. Impacts of a regional, multi-year, multi-species coral disease outbreak in Southeast Florida. Front Mar Sci. 2018;5:1–14.Article 

    Google Scholar 
    Woodhams DC, Bletz MC, Becker CG, Bender HA, Buitrago-Rosas D, Diebboll H, et al. Host-associated microbiomes are predicted by immune system complexity and climate. Genome Biol. 2020;21:1–20.Article 

    Google Scholar 
    Burek KA, Gulland FMD, Sheffield G, Beckmen KB, Keyes E, Spraker TR, et al. Infectious disease and the decline of Steller sea lions (Eumetopias jubatus) in Alaska, USA: Insights from serologic data. J Wildl Dis. 2005;41:512–24.Article 

    Google Scholar 
    Chaloupka M, Balazs GH, Work TM. Rise and Fall over 26 years of a marine epizootic in Hawaiian green sea turtles milani. J Wildl Dis. 2009;45:1138–42.Article 

    Google Scholar 
    NOAA. Stony coral tissue loss disease case definition. 2018. Available online at: https://floridadep.gov/sites/default/file/Copy%20of%20StonyCoralTissueLossDisease_CaseDefinition%20final%2010022018.pdf (accessed September 15, 2020).Estrada-Saldívar N, Molina-Hernández A, Pérez-Cervantes E, Medellín-Maldonado F, González-Barrios FJ, Alvarez-Filip L. Reef-scale impacts of the stony coral tissue loss disease outbreak. Coral Reefs. 2020;39:861–6.Article 

    Google Scholar 
    Heres MM, Farmer BH, Elmer F, Hertler H. Ecological consequences of stony coral tissue loss disease in the Turks and Caicos Islands. Coral Reefs. 2021;40:609–24. https://doi.org/10.1007/s00338-021-02071-4.Article 

    Google Scholar 
    Combs IR, Studivan MS, Eckert RJ, Voss JD. Quantifying impacts of stony coral tissue loss disease on corals in Southeast Florida through surveys and 3D photogrammetry. PLoS ONE. 2021;16:1–17. https://doi.org/10.1371/journal.pone.0252593.CAS 
    Article 

    Google Scholar 
    Estrada-Saldívar N, Quiroga-García BA, Pérez-Cervantes E, Rivera-Garibay OO, Alvarez-Filip L. Effects of the stony coral tissue loss disease outbreak on coral communities and the benthic composition of cozumel reefs. Front Mar Sci. 2021;8:1–13. https://doi.org/10.3389/fmars.2021.632777.Article 

    Google Scholar 
    Brandt ME, Ennis RS, Meiling SS, Townsend J, Cobleigh K, Glahn A, et al. The emergence and initial impact of stony coral tissue loss disease (SCTLD) in the United States Virgin Islands. Front Mar Sci. 2021;1-15. https://doi.org/10.3389/fmars.2021.715329.Florida Keys National Marine Sanctuary. Case definition: Stony Coral Tissue Loss Disease (SCTLD). Silver Spring, MD: National Oceanic and Atmospheric Administration; 2018.Neely KL, Shea CP, Macaulay KA, Hower EK, Dobler MA. Short-and long-term effectiveness of coral disease treatments. Front Mar Sci. 2021;8:1–18. https://doi.org/10.3389/fmars.2021.675349.Article 

    Google Scholar 
    Muller EM, Sartor C, Alcaraz NI, van Woesik R. Spatial epidemiology of the stonycoral-tissue-loss disease in Florida. Front Mar Sci. 2020;7:1–11. https://doi.org/10.3389/fmars.2020.00163.Article 

    Google Scholar 
    Dobbelaere T, Muller EM, Gramer LJ, Holstein DM, Hanert E. Coupled epidemiohydrodynamic modeling to understand the spread of a deadly coral disease in Florida. Front Mar Sci. 2020;7:1–16. https://doi.org/10.3389/fmars.2020.591881.Article 

    Google Scholar 
    Work TM, Weatherby TM, Landsberg JH, Kiryu Y, Cook SM, Peters EC. Viral-like particles are associated with endosymbiont pathology in Florida corals affected by stony coral tissue loss disease. Front Mar Sci. 2021;8:1–18. https://doi.org/10.3389/fmars.2021.750658.Article 

    Google Scholar 
    Veglia, AJ, Beavers K, Van Buren EW, Meiling SS, Muller EM, Smith TB, et al. Novel alphaflexiviridae genomes associated with stony coral tissue loss disease (SCTLD)-affected, disease-exposed and unexposed coral colonies in the U.S. Virgin Islands. Microbiol Resour Announc. 11:e01199-21.Rosales SM, Clark AS, Huebner LK, Ruzicka RR, Muller EM. Rhodobacterales and rhizobiales are associated with stony coral tissue loss disease and its suspected sources of transmission. Front Microbiol. 2020;681.Becker CC, Brandt M, Miller CA, Apprill A. Microbial bioindicators of Stony Coral Tissue Loss Disease identified in corals and overlying waters using a rapid field‐based sequencing approach. Environ Microbiol. 2022;3:1166–82.Article 

    Google Scholar 
    Meyer JL, Castellanos-Gell J, Aeby GS, Häse CC, Ushijima B, Paul VJ. Microbial community shifts associated with the ongoing stony coral tissue loss disease outbreak on the Florida reef tract. Front Microbiol. 2019;10:1–12. https://doi.org/10.3389/fmicb.2019.02244.CAS 
    Article 

    Google Scholar 
    Apprill A, Weber LG, Santoro AE. Distinguishing between microbial habitats unravels ecological complexity in coral microbiomes. mSystems. 2016;1:1–18. https://doi.org/10.1128/mSystems.00143-16.Article 

    Google Scholar 
    Pollock FJ, McMinds R, Smith S, Bourne DG, Willis BL, Medina M, et al. Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny. Nat Commun. 2018;9:1–13. https://doi.org/10.1038/s41467-018-07275-x.CAS 
    Article 

    Google Scholar 
    Brown BE, Bythell JC. Perspectives on mucus secretion in reef corals. Mar Ecol Prog Ser. 2005;296:291–309. https://doi.org/10.3354/meps296291.CAS 
    Article 

    Google Scholar 
    Bourne DG, Morrow KM, Webster NS. Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu Rev Microbiol. 2016;70:317–40. https://doi.org/10.1146/annurev-micro-102215-095440.CAS 
    Article 
    PubMed 

    Google Scholar 
    Ritchie KB. Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser. 2006;322:1–14. https://doi.org/10.3354/meps322001.CAS 
    Article 

    Google Scholar 
    Ainsworth TD, Hoegh-Guldberg O. Bacterial communities closely associated with coral tissues vary under experimental and natural reef conditions and thermal stress. Aquat Biol. 2008;4:289–96. https://doi.org/10.3354/ab00102.Article 

    Google Scholar 
    Work TM, Aeby GS. Microbial aggregates within tissues infect a diversity of corals throughout the Indo-Pacific. Mar Ecol Prog Ser. 2014;500:1–9. https://doi.org/10.3354/meps10698.Article 

    Google Scholar 
    Landsberg JH, Kiryu Y, Peters EC, Wilson PW, Perry N, Waters Y, et al. Stony coral tissue loss disease in Florida is associated with disruption of host–zooxanthellae physiology. Front Mar Sci. 2020;7:1–24. https://doi.org/10.3389/fmars.2020.576013.Article 

    Google Scholar 
    Lima LFO, Weissman M, Reed M, Papudeshi B, Alker AT, Morris MM, et al. Modeling of the coral microbiome: the influence of temperature and microbial network. MBio. 2020;11:e02691-19. https://doi.org/10.1128/mBio.02691-19.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    MacKnight NJ, Cobleigh K, Lasseigne D, Chaves-Fonnegra A, Gutting A, Dimos B, et al. Microbial dysbiosis reflects disease resistance in diverse coral species. Commun Biol. 2021;4:1–11. https://doi.org/10.1038/s42003-021-02163-5.Article 

    Google Scholar 
    Walker WA. Dysbiosis. The microbiota in gastrointestinal pathophysiology. Else-vier Inc. p. 227-32. https://doi.org/10.1016/B978-0-12-804024-9/00025-2.McDevitt-Irwin JM, Baum JK, Garren M, Vega thurber RL. Responses of coral-associated bacterial communities to local and global stressors. Front Mar Sci. 2017;4:1–16. https://doi.org/10.3389/fmars.2017.00262.Article 

    Google Scholar 
    Zaneveld JR, Burkepile DE, Shantz AA, Pritchard CE, McMinds R, Payet JP, et al. Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down to microbial scales. Nat Commun. 2016;7:1–12. https://doi.org/10.1038/ncomms11833.CAS 
    Article 

    Google Scholar 
    Zaneveld JR, McMinds R, Thurber RV. Stress and stability: applying the Anna Karenina principle to animal microbiomes. Nat Microbiol. 2017;2:1–8. https://doi.org/10.1038/nmicrobiol.2017.121.CAS 
    Article 

    Google Scholar 
    Sharp W, Maxwell K. Investigating the ongoing coral disease outbreak in the Florida keys: collecting corals to diagnose the etiological agent (s) and establishing sentinel sites to monitor transmission rates and the spatial progression of the disease. 2018.Meiling SS, Muller EM, Lasseigne D, Rossin A, Veglia AJ, MacKnight N, et al. Variable species responses to experimental stony coral tissue loss disease (SCTLD) exposure. Front Mar Sci. 2021;8:1–12.Article 

    Google Scholar 
    Williams L, Smith TB, Burge CA, Brandt ME. Species-specific susceptibility to white plague disease in three common Caribbean corals. Coral Reefs. 2020;39:27–31. https://doi.org/10.1007/s00338-019-01867-9.Article 

    Google Scholar 
    Ainsworth TD, Krause L, Bridge T, Torda G, Raina J-B, Zakrzewski M, et al. The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. ISME J. 2015;9:2261–74.CAS 
    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 Microb 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.CAS 
    Article 

    Google Scholar 
    Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3. https://doi.org/10.1038/nmeth.3869.CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Yilmaz N, Visagie CM, Houbraken J, Frisvad JC, Samson RA. Polyphasic taxonomy of the genus Talaromyces. Stud Mycol. 2014;78:175–341. https://doi.org/10.1016/j.simyco.2014.08.001.CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Huggett MJ, Apprill A. Coral microbiome database: Integration of sequences reveals high diversity and relatedness of coral-associated microbes. Environ Microbiol Rep. 2019;11:372–85. https://doi.org/10.1111/1758-2229.12686.Article 
    PubMed 

    Google Scholar 
    Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar A, et al. ARB: a software environment for sequence data. Nucleic Acids Res. 2004;32:1363–71. https://doi.org/10.1093/nar/gkh293.CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    McMurdie PJ, Holmes S. Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Comput Biol. 2014;10:1–12. https://doi.org/10.1371/journal.pcbi.1003531.CAS 
    Article 

    Google Scholar 
    Oksanen, J, Blanchet, FG, Friendly, M, Kindt, R,Legendre, P, McGlinn, D, et al. vegan: communityecology package. R package version 25-4. 2019.Clarke, KR, Gorley, RN, Somerfield, PJ, Warwick, RM. Change in marine communities: an approach to statistical analysis and interpretation, 3nd edition. PRIMER-E: Plymouth. 2014.Martin BD, Witten D, Willis AD Modeling microbial abundances and dysbiosis with beta-binomial regression. 2019;1–27. http://arxiv.org/abs/1902.02776.Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–10.CAS 
    Article 

    Google Scholar 
    NOAA. Stony coral tissue loss disease case definition. 2018. p. 1–10.Morrow KM, Moss AG, Chadwick NE, Liles MR. Bacterial associates of two caribbean coral species reveal species-specific distribution and geographic variability. Appl Environ Microbiol. 2012;78:6438–49.CAS 
    Article 

    Google Scholar 
    Glasl B, Herndl GJ, Frade PR. The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance. ISME J. 2016;10:2280–92. https://doi.org/10.1038/ismej.2016.9.CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gardiner M, Bournazos AM, Maturana-Martinez C, Zhong L, Egan S. Exoproteome analysis of the seaweed pathogen Nautella italica R11 reveals temperature-dependent regulation of RTX-like proteins. Front Microbiol. 2017;8:1–9.Article 

    Google Scholar 
    Fernandes N, Case RJ, Longford SR, Seyedsayamdost MR, Steinberg PD, Kjelleberg S, et al. Genomes and virulence factors of novel bacterial pathogens causing bleaching disease in the marine red alga Delisea pulchra. PLoS ONE. 2011;6:e27387. https://doi.org/10.1371/journal.pone.0027387.CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    De O, Santos E, Alves N, Dias GM, Mazotto AM, Vermelho A, et al. Genomic and proteomic analyses of the coral pathogen Vibrio coralliilyticus reveal a diverse virulence repertoire. ISME J. 2011;5:1471–83.Article 

    Google Scholar 
    Viehman S, Mills DK, Meichel GW, Richardson LL. Culture and identification of Desulfovibrio spp. from corals infected by black band disease on Dominican and Florida Keys reefs. Dis Aquat Organ. 2006;69:119–27.CAS 
    Article 

    Google Scholar 
    Brownell AC, Richardson LL. Sulfate reducing bacteria as secondary and necessary pathogens in black band disease of corals. Rev Biol Trop. 2014;62:1–9.Article 

    Google Scholar  More

  • in

    Changes in plant biodiversity facets of rocky outcrops and their surrounding rangelands across precipitation and soil gradients

    Larson, D. W., Matthes, U. & Kelly, P. E. Cliff Ecology (Cambridge University Press, 2000).Book 

    Google Scholar 
    Cooper, A. Plant species coexistence in cliff habitats. J. Biogeogr. 24, 483–494 (1997).Article 

    Google Scholar 
    Davis, P. H. Cliff vegetation in the eastern Mediterranean. J. Ecol. 39, 63–93 (1951).Article 

    Google Scholar 
    Snogerup, S. Evolutionary and plant geographical aspects of chasmophytic communities. In Plant life of South-West Asia (eds Davis, P. H. et al.) 157–170 (Bot. Soc. Edinb, 1971).
    Google Scholar 
    Baskin, J. M. & Baskin, C. C. Endemism in rock outcrop plant communities of unglaciated eastern United States: An evaluation of the roles of the edaphic, genetic and light factors. J. Biogeogr. 15, 829–840 (1988).Article 

    Google Scholar 
    Medina, B. M. O. & Fernandes, G. W. The potential of natural regeneration of rocky outcrop vegetation on rupestrian field soils in Serra do Cipo, Brazil. Braz. J. Bot. 30, 665–678 (2007).Article 

    Google Scholar 
    Alves, R. J. V., Cardin, L. & Kropf, M. S. Angiosperm disjunction “Campos Rupestres-Restingas”: Are-evaluation. Acta Bot. Bras. 2, 675–685 (2007).Article 

    Google Scholar 
    Harley, R. M. Introduction. In Flora of the Pico das Almas, Chapada Diamantina, Bahia, Brazil (eds Stannard, B. L., Harvey, Y. B. & Harley, R. M) 1–42 (Royal Botanic Gardens, 1995).Hubbell, S. P. Neutral theory in ecology and the evolution of ecological equivalence. Ecology 87, 1387–1398 (2006).PubMed 
    Article 

    Google Scholar 
    Conceição, A. A., Pirani, J. R. & Meirelles, S. T. Floristics, structure and soil of insular vegetation in four quartzite-sandstone outcrops of “Chapada Diamantina”, Northeast Brazil. Rev. Bras. Bot. 30, 641–656 (2007).Article 

    Google Scholar 
    Le Stradic, S., Buisson, E. & Wilson, F. G. Vegetation composition and structure of some Neotropical mountain grasslands in Brazil. J Mt Sci 12:864–77. An. Acad. Bras. Ciênc. 87(4), 2097–2110 (2015).Article 
    CAS 

    Google Scholar 
    Nunes, J. A. et al. Soil–vegetation relationships on a banded ironstone ‘island’, Carajás Plateau, Brazilian Eastern Amazonia. An. Acad. Bras. Cienc. 87(4), 2097–2110 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Silva, W. A. Gradiente vegetacional e pedológico em complexo rupestre de quartzito no Quadrilátero Ferrífero, Minas Gerais, Brasil. MSc Thesis. (Universidade Federal de Viçosa, 2013).Vincent, R. C. & Meguro, M. Influence of soil properties on the abundance of plant species in ferruginous rocky soils vegetation, southeastern Brazil. Braz. J. Bot. 31, 377–388 (2008).Article 

    Google Scholar 
    Porembski, S. Tropical inselbergs: Habitat types, adaptive strategies and diversity patterns. Rev. Bras. de Bot. 30, 579–586 (2007).Article 

    Google Scholar 
    De Paula, L. F. A., Forzza, R. C., Neri, A. V., Bueno, M. L. & Porembski, S. Sugar Loaf Land in south-eastern Brazil: A center of diversity for mat-forming bromeliads on inselbergs. Bot. J. Linn. Soc. 181, 459–476 (2016).Article 

    Google Scholar 
    Rezende, M. G., Elias, R. C. L., Salimena, F. R. G. & Neto, L. M. Flora vascular da Serra da Pedra Branca, Caldas, Minas Gerais e relações florísticas com áreas de altitude da Região Sudeste do Brasil. Biota Neotrop. 13, 201–224 (2013).Article 

    Google Scholar 
    Sarthou, C., Villiers, J. F. & Ponge, J. F. Shrub vegetation on tropical granitic inselbergs in French Guiana. J. Veg. Sci. 14, 645–652 (2003).Article 

    Google Scholar 
    Tinti, B. V. et al. Plant diversity on granite/gneiss rock outcrop at Pedra do Pato, Serra do Brigadeiro State Park, Brazil. Check List 11, 1780 (2015).Article 

    Google Scholar 
    Barbara, T., Martinelli, G., Fay, M. F., Mayo, S. J. & Lexer, C. Population differentiation and species cohesion in two closely related plants adapted to neotropical high-altitude “inselbergs”, Alcantarea imperialis and Alcantarea geniculata (Bromeliaceae). Mol. Ecol. 16, 1981–1992 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Boisselier-Dubayle, M. C., Leblois, R., Samadi, S., Lambourdière, J. & Sarthou, C. Genetic structure of the xerophilous bromeliad Pitcairnia geyskesii on inselbergs in French Guiana—A test of the forest refuge hypothesis. Ecography 33, 175–184 (2010).Article 

    Google Scholar 
    Domingues, R. et al. Genetic variability of an endangered Bromeliaceae species (Pitcairnia albiflos) from the Brazilian Atlantic rainforest. Genet. Mol. Res. 10, 2482–2491 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hmeljevski, K. V. et al. Conservation assessment of an extremely restricted bromeliad highlights the need for population-based conservation on granitic inselbergs of the Brazilian Atlantic Forest. Flora Morpho. Distribut. Funct. Ecolo. Plants. 209, 250–259 (2014).Article 

    Google Scholar 
    Palma-Silva, C. et al. Sympatric bromeliad species (Pitcairnia spp.) facilitate tests of mechanisms involved in species cohesion and reproductive isolation in Neotropical inselbergs. Mol. Ecol. 20, 3185–3201 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    Gomes, P. & Alves, M. Floristic diversity of two crystalline rocky outcrops in the Brazilian northeast semi-arid region. Rev. Bras. Bot. 33(4), 661–676 (2010).Article 

    Google Scholar 
    Nunes, J. A., Villa, P. M., Neri, A. V., Silva, W. A. & Schaefer, C. E. G. R. Seasonality drives herbaceous community beta diversity in lithologically different rocky outcrops in Brazil. Plant. Ecol. Evol. 153(2), 208–218 (2020).Article 

    Google Scholar 
    Speziale, K. L. & Ezcurra, C. The role of outcrops in the diversity of Patagonian vegetation: Relicts of glacial palaeofloras?. Flora Morphol. Distrib. Funct. Ecol. Plant. 207, 141–149 (2012).
    Google Scholar 
    Speziale, K. L., Ruggiero, A. & Ezcurra, C. Plant species richness–environment relationships across the Subantarctic-Patagonian transition zone. J. Biogeogr. 37, 449–464 (2010).Article 

    Google Scholar 
    Yates, C. J. et al. High species diversity and turnover in granite inselberg floras highlight the need for a conservation strategy protecting many outcrops. Ecol. Evol. 9, 7660–7675 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Gaston, K. J. Geographic range limits: Achieving synthesis. Proc. R. Soc. B Biol. Sci. 276, 1395–1406 (2009).Article 

    Google Scholar 
    McGann, T. D. How insular are ecological ‘islands’? An example from the granitic outcrops of the New England Batholith of Australia. Proc. R. Soc. Queensland. 110, 1–13 (2002).
    Google Scholar 
    Parmentier, I., Stévart, T. & Hardy, O. J. The inselberg flora of Atlantic Central Africa. I. Determinants of species assemblages. J. Biogeogr. 32, 685–696 (2005).Article 

    Google Scholar 
    Changwe, K. & Balkwill, K. Floristics of the Dunbar Valley serpentinite site, Songimvelo Game Reserve, South Africa. Bot. J. Linn. Soc. 143, 271–285 (2003).Article 

    Google Scholar 
    Clarke, P. J. Habitat islands in fire-prone vegetation: Do landscape features influence community composition?. J. Biogeogr. 29, 677–684 (2002).Article 

    Google Scholar 
    De Bello, F., Leps, J. & Sebastia, M. T. Variations in species and functional plant diversity along climatic and grazing gradients. Ecography 29(6), 801–810 (2006).Article 

    Google Scholar 
    Porembski, S., Martinelli, G., Ohlemüller, R. & Barthlott, W. Diversity and ecology of saxicolous vegetation mats on inselbergs in the Brazilian Atlantic rainforest. Divers. Distrib. 4, 107–119 (1998).Article 

    Google Scholar 
    Porembski, S., Szarzynski, J., Mund, J. P. & Barthlott, W. Biodiversity and vegetation of small-sized inselbergs in a West African rain forest (Taï, Ivory Coast). J. Biogeogr. 23, 47–55 (1996).Article 

    Google Scholar 
    Rahmanian, S. et al. Effects of livestock grazing on soil, plant functional diversity, and ecological traits vary between regions with different climates in northeastern Iran. Ecol. Evol. 9, 8225–8237 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Speziale, K. L. & Ezcurra, C. Patterns of alien plant invasions in northwestern Patagonia, Argentina. J. Arid Environ. 75, 890–897 (2011).ADS 
    Article 

    Google Scholar 
    Qian, H., Chen, S. H. & Zhang, J. L. Disentangling environmental and spatial effects on phylogenetic structure of angiosperm tree communities in China. Sci. Rep. 7, 5864 (2017).ADS 
    Article 
    CAS 

    Google Scholar 
    Farzam, M. & Ejtehadi, H. Effects of drought and canopy facilitation on plant diversity and abundance in a semiarid mountainous rangeland. J. Plant. Ecol. 10(4), 626–633 (2016).
    Google Scholar 
    Heino, J. & Tolonen, K. T. Ecological drivers of multiple facets of beta diversity in a lentic macroinvertebrate metacommunity. Limnol. Oceanogr. 62, 2431–2444. https://doi.org/10.1002/lno.10577 (2017).ADS 
    Article 

    Google Scholar 
    Miranda, J. D., Armas, C., Padilla, F. M. & Pugnaire, F. I. Climatic change and rainfall patterns: Effects on semi-arid plant communities of the Iberian Southeast. J. Arid. Environ. 75, 1302–1309 (2011).ADS 
    Article 

    Google Scholar 
    Pashirzad, M., Ejtehadi, H., Vaezi, J. & Shefferson, R. P. Multiple processes at different spatial scales determine beta diversity patterns in a mountainous semi-arid rangeland of Khorassan-Kopet Dagh floristic province, NE Iran. Plant. Ecol. 220(9), 829–844 (2019).Article 

    Google Scholar 
    Victorero, L., Robert, K., Robinson, L. F., Taylor, M. L. & Huvenne, V. A. I. Species replacement dominates megabenthos beta diversity in a remote seamount setting. Sci. Rep. 8, 4152 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Deil, U. Rock communities in tropical Arabia. Flora et Vegetation Mundi 9, 175–187 (1991).
    Google Scholar 
    Dimopoulos, P., Sýkora, K. V., Mucina, L. & Georgiadis, T. The high-rank syntaxa of the rock-cliff and scree vegetation of the mainland Greece and Crete. Folia Geobot. 32, 313–334 (1997).Article 

    Google Scholar 
    Hein, P., Kürschner, H. & Parolly, G. Phytosociological studies on high mountain plant communities of the Taurus Mountains (Turkey) 2. Rock communities. Phytocoenologia 28, 465–563 (1998).Article 

    Google Scholar 
    Nowak, A., Nowak, S., Nobis, M. & Nobis, A. Vegetation of rock clefts and ledges in the Pamir Alai Mts, Tajikistan (Middle Asia). Cent. Eur. J. Biol. 9, 444–460 (2014).
    Google Scholar 
    Urbis, A. & Blazyca, B. Rock vascular plant species of the Kraków-Częstochowa, Uplands. Thaiszia J. Bot. 21, 207–214 (2011).
    Google Scholar 
    Wiser, S. K., Peet, R. K. & White, P. S. High-elevation rock outcrop vegetation of the Southern Appalachian Mountains. J. Veg. Sci. 7, 703–722 (1996).Article 

    Google Scholar 
    Cadotte, M. W. Experimental evidence that evolutionarily diverse assemblages result in higher productivity. PNAS 110(22), 8996–9000 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Swenson, G.N. Functional and Phylogenetic Ecology in R (Use R!) Kindle Edition (2014).Cadotte, M. W. & Davies, P. R. Why phylogenies do not always predict ecological differences. Ecol. Monogr. 87(4), 535–551 (2016).Article 

    Google Scholar 
    De Bello, F., LepŠ, J. A. N. & Sebastià, M. T. Predictive value of plant traits to grazing along a climatic gradient in the Mediterranean. J. Appl. Ecol. 42(5), 824–833 (2005).Article 

    Google Scholar 
    Funk, J. et al. Revisiting the Holy Grail: Using plant functional traits to understand ecologica processes. Biol. Rev. 92(2), 1156–1173 (2017).PubMed 
    Article 

    Google Scholar 
    Lavorel, S. & Garnier, É. Predicting changes in community composition and ecosystem functioning from plant traits: Revisiting the Holy Grail. Funct. Ecol. 16(5), 545–556 (2002).Article 

    Google Scholar 
    Violle, C. et al. Let the concept of trait be functional!. Oikos 116, 882–892 (2007).Article 

    Google Scholar 
    Zheng, S., Li, W., Lan, Z., Ren, H. & Wang, K. Functional trait responses to grazing are mediated by soil moisture and plant functional group identity. Sci. Rep. 5, 18163 (2015).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Gillison, A. N. Plant functional types and traits at the community, ecosystem and world level. In Vegetation Ecology (eds van der Maarel, E. & Franklin, J.) 347–386 (Wiley, 2013).Chapter 

    Google Scholar 
    Loreau, M. Biodiversity and ecosystem functioning: Recent theoretical advances. Oikos 91, 3–17 (2000).Article 

    Google Scholar 
    Akhani, H., Djamali, M., Ghorbanalizadeh, A. & Ramezani, E. Plant biodiversity of Hyrcanian relict forests, N Iran: An overview of the flora, vegetation, paleoecology and conservation. Pak. J. Bot. 42, 231–258 (2010).
    Google Scholar 
    Hamzehee, B. et al. Phytosociological survey of remnant Alnus glutinosa ssp. barbata communities in the lowland Caspian forests of northern Iran. Pytocoenologia. 38, 117–132 (2008).Article 

    Google Scholar 
    Moradi, H. et al. Elevational gradient and vegetation-environmental relationships in the central Hyrcanian forests of northern Iran. Nord. J. Bot. 34, 1–14 (2016).Article 

    Google Scholar 
    Naqinezhad, A., Esmailpoor, A. & Jafari, N. A new record of Pyrola minor (Pyrolaceae) for the flora of Iran as well as a description of its surrounding habitats. Taxon. Biosyst. 22, 71–80 (2015).
    Google Scholar 
    Naqinezhad, A., Zare-Maivan, H. & Gholizadeh, H. A floristic survey of the Hyrcanian forests in Northern Iran, using two lowland-mountain transects. J. For. Res. 26, 187–199 (2015).CAS 
    Article 

    Google Scholar 
    Sagheb-Talebi, K., Sajedi, T. & Pourhashemi, M. Forests of Iran (Springer Sci, 2014).Book 

    Google Scholar 
    Siadati, S. et al. Botanical diversity of Hyrcanian forests; a case study of a transect in the Kheyrud protected lowland mountain forests in northern Iran. Phytotaxa 7, 1–18 (2010).Article 

    Google Scholar 
    Akhani, H. & Ziegler, H. Photosynthetic pathways and habitats of grasses in Golestan National Park (NE Iran), with an emphasis on the C 4-grass dominated rock communities. Phytocoenologia 32, 455–501 (2002).Article 

    Google Scholar 
    Akhani, H., Mahdavi, P., Noroozi, J. & Zarrinpour, V. Vegetation patterns of the Irano-Turanian steppe along a 3,000 m altitudinal gradient in the Alborz Mountains of Northern Iran. Folia Geobot. 48, 229–255 (2013).Article 

    Google Scholar 
    Klein, J. C. The altitudinal vegetation Alborez The Central (Iran) between the Iranian-Turanian and Euro-Siberian regions (French) (Institut Français de Recherche en Iran, 2001).
    Google Scholar 
    Noroozi, J. Case study: High Mountain Regions in Iran 255–260. of Chapter 7 (Endemism in mainland regions-case studies). In Endemism in Vascular plants. Plant. Veg. (ed Hobohm, C.) 9. (Springer, 2014).Noroozi, J., Akhani, H. & Willner, W. Phytosociological and ecological study of the high alpine vegetation of Tuchal Mountains (Central Alborz, Iran). Phytocoenologia 40, 293–321 (2010).Article 

    Google Scholar 
    Do Carmo, F. F. & Jacobi, C. M. Diversity and plant trait-soil relationships among rock outcrops in the Brazilian Atlantic rainforest. Plant Soil. 403, 7–20 (2015).Article 
    CAS 

    Google Scholar 
    Cavender-Bares, J., Kozak, K. H., Fine, P. V. A. & Kembel, S. The merging of community ecology and phylogenetic biology. Ecol Lett. 12, 693–715 (2009).PubMed 
    Article 

    Google Scholar 
    Heydari, M., Poorbabaei, H., Esmailzadeh, O., Salehi, A. & EshaghiRad, J. Indicator plant species in monitoring forest soil conditions using logistic regression model in Zagros Oak (Quercus brantii var. persica) forest ecosystems. Ilam city. J. Plant Res. 27(5), 811–828 (2014).
    Google Scholar 
    Speziale, K. L. & Ezcurra, C. Rock outcrops as potential biodiversity refugia under climate change in North Patagonia. Plant Ecol. Diver. 8, 353–361 (2014).Article 

    Google Scholar 
    Rahmanian, S. et al. Effects of livestock grazing on plant species diversity vary along a climatic gradient in northeastern Iran. Appl. Veg. Sci. 23, 551–561 (2020).Article 

    Google Scholar 
    Huston, M. A. Biological Diversity: The Coexistence of Species in Changing Landscape (Cambridge University, 1994).
    Google Scholar 
    Mason, N. W., Mouillot, D. & Lee, W. G. Functional richness, functional evenness and functional divergence: The primary components of functional diversity. Oikos 111, 112–118 (2005).Article 

    Google Scholar 
    Stubbs, W. J. & Wilson, J. B. Evidence for limiting similarity in a sand dune community. J. Ecol. 92, 557567 (2004).Article 

    Google Scholar 
    Stanisci, A. et al. Functional composition and diversity of leaf traits in subalpine versus alpine vegetation in the Apennines. Ann. Bot. Comp. plants. 12, plaa004 (2020).CAS 

    Google Scholar 
    Chesson, P. et al. Resource pulses, species interactions, and diversity maintenance in arid and semi-arid environments. Oecologia 141, 236–253 (2004).ADS 
    PubMed 
    Article 

    Google Scholar 
    Rosbakh, S. et al. Contrasting effects of extreme drought and snowmelt patterns on mountain plants along an elevation gradient. Front. Plant Sci. 8, 1478 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Korner, C. Alpine Treelines: Functional Ecology of the Global High Elevation tree Limits (Springer Sci. & Business Media, 2012).Book 

    Google Scholar 
    Reich, P. B. et al. Generality of leaf trait relationships: A test across six biomes. Ecology 80, 1955–1969 (1999).Article 

    Google Scholar 
    Westoby, M., Falster, D. S., Moles, A. T., Vesk, P. A. & Wright, I. J. Plant ecological strategies: Some leading dimensions of variation between species. Ann. Rev. Ecol. Syst. 33, 125–159 (2002).Article 

    Google Scholar 
    Hautier, Y., Niklaus, P. A. & Hector, A. Competition for light causes plant biodiversity loss after eutrophication. Science 324, 636–638 (2009).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    De Bello, F. D. et al. Hierarchical effects of environmental filters on the functional structure of plant communities: A case study in the French Alps. Ecography 36, 393–402 (2013).Article 

    Google Scholar 
    Korner, C., Neumayer, M., Menendez-Riedl, S. P. & Smeets-Scheel, A. Functional morphology of mountain plants. Flora 182, 353–383 (1989).Article 

    Google Scholar 
    Rosbakh, S., Römermann, C. & Poschlod, P. Specific leaf area correlates with temperature new evidence of trait variation at the population, species and community levels. Alp. Bot. 125, 79–86 (2015).Article 

    Google Scholar 
    Ordonez, J. C. et al. Global study of relationships between leaf traits, climate and soil measures of nutrient fertility. Glob. Ecol. Biogeogr. 18, 137–149 (2009).Article 

    Google Scholar 
    Li, W. et al. Community-weighted mean traits but not functional diversity determine the changes in soil properties during wetland drying on the Tibetan Plateau. Solid Earth. 8, 137–147 (2017).ADS 
    Article 

    Google Scholar 
    Bardgett, R. D., Mommer, L. & De Vries, F. T. Going underground: Root traits as drivers of ecosystem processes. Trends Ecol. Evol. 29, 692–699 (2014).PubMed 
    Article 

    Google Scholar 
    Lane, D. R., Coffin, D. P. & Lauenroth, W. K. Effects of soil texture and precipitation on above-ground net primary productivity and vegetation structure across the Central Grassland region of the United States. J. Veg. Sci. 9, 239–250 (1998).Article 

    Google Scholar 
    Noy-Meir, I. Multivariate analysis of the semi-arid vegetation of southern Australia. II. Vegetation catenae an environmental gradients. Aust. J. Bot. 22, 40–115 (1973).
    Google Scholar 
    Moura, M. R., Villalobos, F., Costa, G. C. & Garcia, P. C. A. Disentangling the role of climate, topography and vegetation in species richness gradients. PLoS ONE 11(3), 0152468 (2016).Article 
    CAS 

    Google Scholar 
    Neri, A. V. et al. Soil and altitude drives diversity and functioning of Brazilian Páramos (Campo de Altitude). J. plant. Ecol. 10(5), 771–779 (2016).
    Google Scholar 
    Benites, V. M., Schaefer, C. E. G. R., Simas, F. N. B., Santos, H. G. & Mendonca, B. A. F. Soils associated to rock outcrops in the Brazilian mountain ranges Mantiqueira and Espinhaço. Rev. Bras. Bot. 30, 569–577 (2007).Article 

    Google Scholar 
    Flynn, D. F. B. et al. Loss of functional diversity under land use intensification across multiple taxa. Ecol. Lett. 12, 22–33 (2009).PubMed 
    Article 

    Google Scholar 
    Zuo, X. A. et al. Testing associations of plant functional diversity with along a restoration gradient of sandy grassland. Front. Plant. Sci. 7, 1–11 (2016).ADS 
    Article 

    Google Scholar 
    Myers-Smith, I. H. et al. Shrub expansion in tundra ecosystems: Dynamics, impacts and research priorities. Environ. Res. Lett. 6, 045509 (2011).ADS 
    Article 

    Google Scholar 
    Vankoughnett, M. R. & Grogan, P. Nitrogen isotope tracer acquisition in low and tall birch tundra plant communities: A 2-year test of the snow–shrub hypothesis. Biogeochemistry 118, 291–306 (2014).CAS 
    Article 

    Google Scholar 
    Pescador, D. S., de Bello, F., Valladares, F. & Escudero, A. Plant trait variation along an altitudinal gradient in Mediterranean high mountain grasslands: Controlling the species turnover effect. PLoS ONE 10, e0118876 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Pescador, D. S., Sierra-Almeida, A., Torres, P. J. & Escudero, A. Summer freezing resistance: A critical filter for plant community assemblies in Mediterranean high mountains. Front. Plant. Sci. 7, 194 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Heydarnejad, S. & Ranjbar, A. Investigation of the effect of salinity stress on growth characteristic and ion accumulation in plants. J. Desert Ecos. Eng. 3(4), 1–10 (2013).
    Google Scholar 
    Perez-Harguindeguy, N. et al. New handbook for standardized measurement of plant functional traits worldwide. Aust. J. Bot. 61, 167–234 (2013).Article 

    Google Scholar 
    Cornelissen, J. H. C. et al. A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust. J. Bot. 51, 335–380 (2003).Article 

    Google Scholar 
    Raunkiaer, C. The Life Forms of Plants and Statistical Plant Geography (Oxford University Press, 1934).
    Google Scholar 
    Gee, G. W. & Bauder, J. W. Particle size analysis. In Methods of Soil Analysis. Part 1, 2nd ed. (ed Klute, A.) Agronomy Monographs, Vol. 9, 383–409 (Am. Soc. Agr., 1986).Bremner, J. M. In Nitrogen-Total Methods of Soil Analysis. (eds Sparks, D. L.) Soil Sci Soc Am J. 1085–1122 (Am Soc Agr. Inc, 1996).Walkley, A. & Black, I. A. An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci. 37, 29–38 (1934).ADS 
    CAS 
    Article 

    Google Scholar 
    Nelson, D. W. & Sommers, L. Total carbon, organic carbon, and organic matter 1. Methods of soil analysis. Part 2. Chemical and microbi‐ological properties, (methodsofsoilan2), 539–579 (1982).Miller, R. H. & Keeney, D. R. Methods of soil analysis, 2nd ed. In Part 2. Chemical and Microbiological Properties (eds Page, A. L. et al.) 1–129 (ASA, SSSA, 1982).
    Google Scholar 
    Food and Agriculture Organization-FAO. Management of gypsiferous soils. Soil Bulletin, 62, (FAO, 1990).Chao, A. et al. Rarefaction and extrapolation with Hill numbers: A framework for sampling and estimation in species diversity studies. Ecol. Monogr. 84, 45–67 (2014).Article 

    Google Scholar 
    Shipley, B., Vile, D. & Garnier, É. from plant traits to plant communities: A statistica mechanistic approach to biodiversity. Science 314(5800), 812–814 (2006).ADS 
    MathSciNet 
    CAS 
    PubMed 
    MATH 
    Article 

    Google Scholar 
    Zhu, J., Jiang, L. & Zhang, Y. Relationships between functional diversity and aboveground biomass production in the Northern Tibetan alpine grasslands. Sci. Rep. 6, 34105 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Laliberte, E. & Legendre, P. A distance-based framework for measuring functional diversity from multiple traits. Ecology 91(1), 299–305 (2010).PubMed 
    Article 

    Google Scholar 
    Wheeler, D. & Tiefelsdorf, M. Multicollinearity and correlation among local regression coefficients in geographically weighted regression. J. Geogr. Syst. 7, 161–187 (2005).Article 

    Google Scholar 
    Fox, J. & Weisberg, S. A review of: an R companion to applied regression, second edition. J. Biopharm. Stat. 22, 418–419 (2011).
    Google Scholar 
    Brien, R. M. A caution regarding rules of thumb for variance inflation factors. Qual. Quant. 41, 673–690 (2007).Article 

    Google Scholar 
    Dray, S., Legendre, P. & Blanchet, F. G. packfor: forward selection with permutation (Canoco p. 46). (2011) http://R-Forge.R-project.org/projects/sedar (Accessed 7 Nov 2016).Blanchet, F. G., Legendre, P. & Borcard, D. Forward selection of explanatory variables. Ecology 89, 2623–2632 (2008).PubMed 
    Article 

    Google Scholar 
    Oksanen, J. et al. vegan: Community Ecology Package (2017).Wickham, H. et al. Ggplot2: Elegant Graphics for Data Analysis 2nd edn. (Springer International Publishing, 2016).MATH 
    Book 

    Google Scholar  More

  • in

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

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

  • in

    Shoaling guppies evade predation but have deadlier parasites

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

    Google Scholar  More

  • in

    A trait database and updated checklist for European subterranean spiders

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

  • in

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

    Google Scholar  More

  • in

    Reply to: Assessing the efficiency of Verily’s automated process for production and release of male Wolbachia-infected mosquitoes

    Crawford, J. E. et al. Efficient production of male Wolbachia-infected Aedes aegypti mosquitoes enables large-scale suppression of wild populations. Nat. Biotechnol. 38, 482–492 (2020).CAS 
    Article 

    Google Scholar 
    Xi, Z., Khoo, C. C. H. & Dobson, S. L. Wolbachia establishment and invasion in an Aedes aegypti laboratory population. Science 310, 326–328 (2005).CAS 
    Article 

    Google Scholar 
    Phuc, H. K. et al. Late-acting dominant lethal genetic systems and mosquito control. BMC Biol. 5, 11 (2007).Article 

    Google Scholar 
    Kandul, N. P. et al. Transforming insect population control with precision guided sterile males with demonstration in flies. Nat. Commun. 10, 84 (2019).CAS 
    Article 

    Google Scholar 
    Kyrou, K. et al. A CRISPR–Cas9 gene drive targeting doublesex causes complete population suppression in caged Anopheles gambiae mosquitoes. Nat. Biotechnol. 36, 1062–1066 (2018).CAS 
    Article 

    Google Scholar 
    Kittayapong, P. et al. Combined sterile insect technique and incompatible insect technique: the first proof-of-concept to suppress Aedes aegypti vector populations in semi-rural settings in Thailand. PLoS Negl. Trop. Dis. 13, e0007771 (2019).Article 

    Google Scholar 
    Zheng, X. et al. Incompatible and sterile insect techniques combined eliminate mosquitoes. Nature 572, 56–61 (2019).CAS 
    Article 

    Google Scholar 
    Ryan, P. A. et al. Establishment of wMel Wolbachia in Aedes aegypti mosquitoes and reduction of local dengue transmission in Cairns and surrounding locations in northern Queensland, Australia. Gates Open Res. 3, 1547 (2019).Article 

    Google Scholar 
    Indriani, C. et al. Reduced dengue incidence following deployments of Wolbachia-infected Aedes aegypti in Yogyakarta, Indonesia: a quasi-experimental trial using controlled interrupted time series analysis. Gates Open Res. 4, 50 (2020).Velez, I. D. et al. The impact of city-wide deployment of Wolbachia-carrying mosquitoes on arboviral disease incidence in Medellín and Bello, Colombia: study protocol for an interrupted time-series analysis and a test-negative design study. F1000Res. 8, 1327 (2020).Article 

    Google Scholar 
    Durovni, B. et al. The impact of large-scale deployment of Wolbachia mosquitoes on dengue and other Aedes-borne diseases in Rio de Janeiro and Niterói, Brazil: study protocol for a controlled interrupted time series analysis using routine disease surveillance data. F1000Res. 8, 1328 (2020).Article 

    Google Scholar 
    O’Connor, L. et al. Open release of male mosquitoes infected with a Wolbachia biopesticide: field performance and infection containment. PLoS Negl. Trop. Dis. 6, e1797 (2012).Article 

    Google Scholar 
    Nazni, W. A. et al. Establishment of Wolbachia strain wAlbB in Malaysian populations of Aedes aegypti for dengue control. Curr. Biol. 29, 4241–4248 (2019).CAS 
    Article 

    Google Scholar 
    Klassen, W. & Curtis, C. F. In: Sterile Insect Technique (eds Dyck, V. A., Hendrichs, J. & Robinson, A. S.) 3–36 (Springer-Verlag, 2005).Fried, M. Determination of sterile-insect competitiveness. J. Econ. Entomol. 64, 869–872 (1971).Article 

    Google Scholar 
    Bouyer, J. et al. Field performance of sterile male mosquitoes released from an uncrewed aerial vehicle. Sci. Robot. 5, eaba6251 (2020).Article 

    Google Scholar 
    Krafsur, E. S., Whitten, C. J. & Novy, J. E. Screwworm eradication in North and Central America. Parasitol. Today 3, 131–137 (1987).CAS 
    Article 

    Google Scholar 
    Hendrichs, J., Ortiz, G., Liedo, P. & Schwarz, A. Six years of successful medfly program in Mexico and Guatemala. In: Fruit Flies of Economic Importance (ed Cavalloro, R.) 353–365 (A. A. Balkema, 1983).Helinski, M. E. H., Parker, A. G. & Knols, B. G. J. Radiation-induced sterility for pupal and adult stages of the malaria mosquito Anopheles arabiensis. Malar. J. 5, 41 (2006).Article 

    Google Scholar 
    Helinski, M. E. H., Parker, A. G. & Knols, B. G. J. Radiation biology of mosquitoes. Malar. J. 8 Suppl 2, S6 (2009).Benedict, M. Q. & Robinson, A. S. The first releases of transgenic mosquitoes: an argument for the sterile insect technique. Trends Parasitol. 19, 349–355 (2003).Article 

    Google Scholar 
    Culbert, N. J. et al. Longevity of mass-reared, irradiated and packed male Anopheles arabiensis and Aedes aegypti under simulated environmental field conditions. Parasit. Vectors 11, 603 (2018).CAS 
    Article 

    Google Scholar 
    Culbert, N. J. et al. A rapid quality control test to foster the development of genetic control in mosquitoes. Sci. Rep. 8, 16179 (2018).Article 

    Google Scholar 
    Bentley, D. R. et al. Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456, 53–59 (2008).CAS 
    Article 

    Google Scholar 
    Carlson, R. The pace and proliferation of biological technologies. Biosecur. Bioterror. 1, 203–214 (2003).Article 

    Google Scholar 
    The Wolbachia Project–Singapore Consortium & Ching, N. L. Wolbachia-mediated sterility suppresses Aedes aegypti populations in the urban tropics. Preprint at https://www.medrxiv.org/content/10.1101/2021.06.16.21257922v1 (2021).Soh, S. et al. Economic impact of dengue in Singapore from 2010 to 2020 and the cost-effectiveness of Wolbachia interventions. PLoS Global Public Health https://doi.org/10.1371/journal.pgph.0000024 (2021). More