More stories

  • in

    A comprehensive database of amphibian heat tolerance

    Arias, P. A. et al. Technical summary. in Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change (2021).Pinsky, M. L., Eikeset, A. M., McCauley, D. J., Payne, J. L. & Sunday, J. M. Greater vulnerability to warming of marine versus terrestrial ectotherms. Nature 569, 108–111 (2019).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Sunday, J. M., Bates, A. E. & Dulvy, N. K. Thermal tolerance and the global redistribution of animals. Nat. Clim. Chang. 2, 686–690 (2012).ADS 
    Article 

    Google Scholar 
    Fry, F. Effects of the environment on animal activity. Publ. Ontario Fish. Res. Lab. 55, 1–62 (1947).
    Google Scholar 
    Lutterschmidt, W. I. & Hutchison, V. H. The critical thermal maximum: history and critique. Can. J. Zool. 75, 1561–1574, https://doi.org/10.1139/z97-783 (2011).Article 

    Google Scholar 
    Rezende, E. L., Castañeda, L. E. & Santos, M. Tolerance landscapes in thermal ecology. Funct. Ecol. 28, 799–809 (2014).Article 

    Google Scholar 
    Bozinovic, F., Calosi, P. & Spicer, J. I. Physiological correlates of geographic range in animals. Annu. Rev. Ecol. Evol. S. 42, 155–179 (2011).Article 

    Google Scholar 
    Sunday, J. M. et al. Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation. Proc. Natl. Acad. Sci. USA 111, 5610–5615 (2014).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Deutsch, C. A. et al. Impacts of climate warming on terrestrial ectotherms across latitude. Proc. Natl. Acad. Sci. USA 105, 6668–6672 (2008).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Comte, L. & Olden, J. D. Climatic vulnerability of the world’s freshwater and marine fishes. Nat. Clim. Chang. 7, 718–722 (2017).ADS 
    Article 

    Google Scholar 
    Dahlke, F. T., Wohlrab, S., Butzin, M. & Pörtner, H.-O. Thermal bottlenecks in the life cycle define climate vulnerability of fish. Science 369, 65–70 (2020).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Pottier, P., Burke, S., Drobniak, S. M. & Nakagawa, S. Methodological inconsistencies define thermal bottlenecks in fish life cycle: a comment on Dahlke et al. 2020. Evol. Ecol. 36, 287–292 (2022).Article 

    Google Scholar 
    Dahlke, F., Butzin, M., Wohlrab, S. & Pörtner, H.-O. Reply to: methodological inconsistencies define thermal bottlenecks in fish life cycle. Evol. Ecol. 36, 293–298 (2022).Article 

    Google Scholar 
    Pottier, P. et al. Developmental plasticity in thermal tolerance: Ontogenetic variation, persistence, and future directions. Ecol. Lett. (2022).Morley, S. A., Peck, L. S., Sunday, J. M., Heiser, S. & Bates, A. E. Physiological acclimation and persistence of ectothermic species under extreme heat events. Glob. Ecol. Biogeogr. 28, 1018–1037 (2019).Article 

    Google Scholar 
    Rohr, J. R. et al. The complex drivers of thermal acclimation and breadth in ectotherms. Ecol. Lett. 21, 1425–1439 (2018).PubMed 
    Article 

    Google Scholar 
    Gunderson, A. R. & Stillman, J. H. Plasticity in thermal tolerance has limited potential to buffer ectotherms from global warming. Proc. R. Soc. B-Biol. Sci. 282, 20150401 (2015).Article 

    Google Scholar 
    Weaving, H., Terblanche, J. S., Pottier, P. & English, S. Meta-analysis reveals weak but pervasive plasticity in insect thermal limits. Nat. Commun. 13, 1–11 (2022).Article 

    Google Scholar 
    Araújo, M. B. et al. Heat freezes niche evolution. Ecol. Lett. 16, 1206–1219 (2013).PubMed 
    Article 

    Google Scholar 
    Bennett, J. M. et al. The evolution of critical thermal limits of life on Earth. Nat. Commun. 12, 1198 (2021).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hoffmann, A. A., Chown, S. L. & Clusella-Trullas, S. Upper thermal limits in terrestrial ectotherms: how constrained are they? Funct. Ecol. 27, 934–949 (2013).Article 

    Google Scholar 
    Kellermann, V. et al. Upper thermal limits of Drosophila are linked to species distributions and strongly constrained phylogenetically. Proc. Natl. Acad. Sci. USA 109, 16228–16233 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Morgan, R., Finnøen, M. H., Jensen, H., Pélabon, C. & Jutfelt, F. Low potential for evolutionary rescue from climate change in a tropical fish. Proc. Natl. Acad. Sci. USA 117, 33365–33372 (2020).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bennett, J. M. et al. GlobTherm, a global database on thermal tolerances for aquatic and terrestrial organisms. Sci. Data 5, 180022 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Leiva, F. P., Calosi, P. & Verberk, W. C. E. P. Scaling of thermal tolerance with body mass and genome size in ectotherms: a comparison between water- and air-breathers. Philos. Trans. R. Soc. B-Biol. Sci. 374, 20190035 (2019).Article 

    Google Scholar 
    Clusella-Trullas, S., Blackburn, T. M. & Chown, S. L. Climatic predictors of temperature performance curve parameters in ectotherms imply complex responses to climate change. Am. Nat. 177, 738–751 (2011).PubMed 
    Article 

    Google Scholar 
    Nakagawa, S. & Freckleton, R. P. Missing inaction: the dangers of ignoring missing data. Trends Ecol. Evol. 23, 592–596 (2008).PubMed 
    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 
    Foo, Y. Z., O’Dea, R. E., Koricheva, J., Nakagawa, S. & Lagisz, M. A practical guide to question formation, systematic searching and study screening for literature reviews in ecology and evolution. Methods Ecol. Evol. 12, 1705–1720 (2021).Article 

    Google Scholar 
    Reboredo Segovia, A. L., Romano, D. & Armsworth, P. R. Who studies where? Boosting tropical conservation research where it is most needed. Front. Ecol. Environ. 18, 159–166 (2020).Article 

    Google Scholar 
    White, C. R. et al. Geographical bias in physiological data limits predictions of global change impacts. Funct. Ecol. 35, 1572–1578 (2021).Article 

    Google Scholar 
    Amano, T., González-Varo, J. P. & Sutherland, W. J. Languages are still a major barrier to global Science. PLoS Biol. 14, e2000933 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bennett, S., Duarte, C. M., Marbà, N. & Wernberg, T. Integrating within-species variation in thermal physiology into climate change ecology. Philos. Trans. R. Soc. B-Biol. Sci. 374, 20180550 (2019).Article 

    Google Scholar 
    Noble, D. W. A. et al. Meta-analytic approaches and effect sizes to account for ‘nuisance heterogeneity’ in comparative physiology. J. Exp. Biol. 225, jeb243225 (2022).PubMed 
    Article 

    Google Scholar 
    Peralta-Maraver, I. & Rezende, E. L. Heat tolerance in ectotherms scales predictably with body size. Nat. Clim. Chang. 11, 58–63 (2021).ADS 
    Article 

    Google Scholar 
    McKenzie, D. J. et al. Intraspecific variation in tolerance of warming in fishes. J. Fish Biol. 98, 1536–1555 (2021).PubMed 
    Article 

    Google Scholar 
    Morrissey, M. B. Meta-analysis of magnitudes, differences and variation in evolutionary parameters. J. Evol. Biol. 29, 1882–1904 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Duffy, G. A., Kuyucu, A. C., Hoskins, J. L., Hay, E. M. & Chown, S. L. Adequate sample sizes for improved accuracy of thermal trait estimates. Funct. Ecol. 35, 2647–2662 (2021).CAS 
    Article 

    Google Scholar 
    IUCN. The IUCN Red List of Threatened Species. https://www.iucnredlist.org (2021).Harfoot, M. B. J. et al. Using the IUCN Red List to map threats to terrestrial vertebrates at global scale. Nat. Ecol. Evol. 5, 1510–1519 (2021).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Sodhi, N. K. et al. Measuring the meltdown: Drivers of global amphibian extinction and decline. PLoS One 3 (2008).Nowakowski, A. J. et al. Tropical amphibians in shifting thermal landscapes under land-use and climate change. Conserv. Physiol. 31, 96–105 (2017).
    Google Scholar 
    Jenkins, C. N., Pimm, S. L. & Joppa, L. N. Global patterns of terrestrial vertebrate diversity and conservation. Proc. Natl. Acad. Sci. USA 110, E2602–E2610 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ouzzani, M., Hammady, H., Fedorowicz, Z. & Elmagarmid, A. Rayyan—a web and mobile app for systematic reviews. Syst. Rev. 5, 210 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Vera-Baceta, M.-A., Thelwall, M. & Kousha, K. Web of Science and Scopus language coverage. Scientometrics 121, 1803–1813 (2019).Article 

    Google Scholar 
    Giustini, D. & Boulos, M. N. K. Google Scholar is not enough to be used alone for systematic reviews. Online J. Public Health Inform. 5, 214 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Haddaway, N. R., Collins, A. M., Coughlin, D. & Kirk, S. The role of Google Scholar in evidence reviews and its applicability to grey literature searching. PLoS One 10, e0138237 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Gusenbauer, M. & Haddaway, N. R. Which academic search systems are suitable for systematic reviews or meta-analyses? Evaluating retrieval qualities of Google Scholar, PubMed, and 26 other resources. Res. Synth. Methods 11, 181–217 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Harzing, A. Publish or perish. Res. Int. Manag. Softw. Release 27 (2007).Cheng, C.-B. A study of warming tolerance and thermal acclimation capacity of tadpoles in Taiwan. (Tunghai University, 2017).Wu, Q.-H. & Hsieh, C.-H. Thermal tolerance and population genetics of Hynobius fuca. (Chinese Culture University, 2016).Jørgensen, L. B., Malte, H., Ørsted, M., Klahn, N. A. & Overgaard, J. A unifying model to estimate thermal tolerance limits in ectotherms across static, dynamic and fluctuating exposures to thermal stress. Sci. Rep. 11, 1–14 (2021).Article 

    Google Scholar 
    Agudelo-Cantero, G. A. & Navas, C. A. Interactive effects of experimental heating rates, ontogeny and body mass on the upper thermal limits of anuran larvae. J. Therm. Biol. 82, 43–51 (2019).PubMed 
    Article 

    Google Scholar 
    Alveal Riquelme, N. Relaciones entre la fisiología térmica y las características bioclimáticas de Rhinella spinulosa (Anura: Bufonidae) en Chile a través del enlace mecanicista de nicho térmico. (Universidad de Concepción, 2015).Alves, M. Tolerância térmica em espécies de anuros neotropicais do gênero Dendropsophus Fitzinger, 1843 e efeito da temperatura na resposta à predação. (Universidade Estadual de Santa Cruz, 2016).Anderson, R. C. O. & Andrade, D. V. Trading heat and hops for water: Dehydration effects on locomotor performance, thermal limits, and thermoregulatory behavior of a terrestrial toad. Ecol. Evol. 7, 9066–9075 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Aponte Gutiérrez, A. Endurecimiento térmico en Pristimantis medemi (Anura: Craugastoridae), en coberturas boscosas del Municipio de Villavicencio (Meta). (Universidad Nacional de Colombia, 2020).Arrigada García, K. Conductas térmica en dos poblaciones de Batrachyla taeniata provenientes de la localidad de Ucúquer en la región de O’Higgins y de la localidad de Hualpén en la región del Bío-Bío (Universidad de Concepción, 2019).Azambuja, G., Martins, I. K., Franco, J. L. & Santos, T. Gdos Effects of mancozeb on heat shock protein 70 (HSP70) and its relationship with the thermal physiology of Physalaemus henselii (Peters, 1872) tadpoles (Anura: Leptodactylidae). J. Therm. Biol. 98, 102911 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bacigalupe, L. D. et al. Natural selection on plasticity of thermal traits in a highly seasonal environment. Evol. Appl. 11, 2004–2013 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Barria, A. M. & Bacigalupe, L. D. Intraspecific geographic variation in thermal limits and acclimatory capacity in a wide distributed endemic frog. J. Therm. Biol. 69, 254–260 (2017).PubMed 
    Article 

    Google Scholar 
    Beltrán, I., Ramírez-Castañeda, V., Rodríguez-López, C., Lasso, E. & Amézquita, A. Dealing with hot rocky environments: critical thermal maxima and locomotor performance in Leptodactylus lithonaetes (anura: Leptodactylidae). Herpetol. J. 29, 155–161 (2019).Article 

    Google Scholar 
    Berkhouse, C. & Fries, J. Critical thermal maxima of juvenile and adult San Marcos salamanders (Eurycea nana). Southwest. Nat. 40, 430–434 (1995).
    Google Scholar 
    Blem, C. R., Ragan, C. A. & Scott, L. S. The thermal physiology of two sympatric treefrogs Hyla cinerea and Hyla chrysoscelis (Anura; Hylidae). Comp. Biochem. Physiol. 85, 563–570 (1986).CAS 
    Article 

    Google Scholar 
    Bonino, M. F., Cruz, F. B. & Perotti, M. G. Does temperature at local scale explain thermal biology patterns of temperate tadpoles? J. Therm. Biol. 94 (2020).Bovo, R. P. Fisiologia térmica e balanço hídrico em anfíbios anuros. (Universidad Estadual Paulista, 2015).Brattstrom, B. H. Thermal acclimation in Australian amphibians. Comp. Biochem. Physiol. 35, 69–103 (1970).Article 

    Google Scholar 
    Brattstrom, B. H. & Regal, P. Rate of thermal acclimation in the Mexican salamander. Chiropterotriton. Copeia 1965, 514–515 (1965).Article 

    Google Scholar 
    Brattstrom, B. H. A preliminary review of the thermal requirements of amphibians. Ecology 44, 238–255 (1963).Article 

    Google Scholar 
    Brattstrom, B. H. Thermal acclimation in anuran amphibians as a function of latitude and altitude. Comp. Biochem. Physiol. 24, 93–111 (1968).CAS 
    PubMed 
    Article 

    Google Scholar 
    Brattstrom, B. H. & Lawrence, P. The rate of thermal acclimation in anuran amphibians. Physiol. Zool. 35, 148–156 (1962).Article 

    Google Scholar 
    Brown, H. A. The heat resistance of some anuran tadpoles (Hylidae and Pelobatidae). Copeia 1969, 138 (1969).Article 

    Google Scholar 
    Burke, E. M. & Pough, F. H. The role of fatigue in temperature resistance of salamanders. J. Therm. Biol. 1, 163–167 (1976).Article 

    Google Scholar 
    Burrowes, P. A., Navas, C. A., Jiménez-Robles, O., Delgado, P. & De La Riva, I. Climatic heterogeneity in the Bolivian andes: Are frogs trapped? S. Am. J. Herpetol. 18, 1–12 (2020).Article 

    Google Scholar 
    Bury, R. B. Low thermal tolerances of stream amphibians in the Pacific Northwest: Implications for riparian and forest management. Appl. Herpetol. 5, 63–74 (2008).Article 

    Google Scholar 
    Castellanos García, L. A. Days of futures past: Integrating physiology, microenvironments, and biogeographic history to predict response of frogs in neotropical dry-forest to global warming. (Universidad de los Andes, 2017).Castro, B. Influence of environment on thermal ecology of direct-developing frogs (Anura: Craugastoridae: Pristimantis) in the eastern Andes of Colombia. (Universidad de los Andes, 2019).Catenazzi, A., Lehr, E. & Vredenburg, V. T. Thermal physiology, disease, and amphibian declines on the eastern slopes of the Andes. Conserv. Biol. 28, 509–517 (2014).PubMed 
    Article 

    Google Scholar 
    Chang, L.-W. Heat tolerance and its plasticity in larval Bufo bankorensis from different altitudes. (National Cheng Kung University, 2002).Chavez Landi, P. A. Fisiología térmica de un depredador Dasythemis sp. (Odonata: Libellulidae) y su presa Hypsiboas pellucens (Anura: Hylidae) y sus posibles implicaciones frente al cambio climático. (Pontificia Universidad Católica Del Ecuador, 2017).Chen, T.-C., Kam, Y.-C. & Lin, Y.-S. Thermal physiology and reproductive phenology of Buergeria japonica (Rhacophoridae) breeding in a stream and a geothermal hotspring in Taiwan. Zool. Sci. 18, 591–596 (2001).Article 

    Google Scholar 
    Cheng, Y.-J. Effect of salinity on the critical thermal maximum of tadpoles living in brackish water. (Tunghai University, 2017).Christian, K. A., Nunez, F., Clos, L. & Diaz, L. Thermal relations of some tropical frogs along an altitudinal gradient. Biotropica 20, 236–239 (1988).Article 

    Google Scholar 
    Claussen, D. L. The thermal relations of the tailed frog, Ascaphus truei, and the pacific treefrog, Hyla regilla. Comp. Biochem. Physiol. 44, 137–153 (1973).Article 

    Google Scholar 
    Claussen, D. L. Thermal acclimation in ambystomatid salamanders. Comp. Biochem. Physiol. 58, 333–340 (1977).Article 

    Google Scholar 
    Contreras Cisneros, J. Temperatura crítica máxima, tolerancia al frío y termopreferendum del tritón del Montseny (Calotriton arnoldii). (Universitat de Barcelona, 2019).Contreras Oñate, S. Posible efecto de las temperaturas de aclimatación sobre las respuestas térmicas en temperaturas críticas máximas (TCmás) y mínimas (TCmín) de una población de Batrachyla taeniata (Universidad de Concepción, 2016).Cooper, R. D. & Shaffer, H. B. Allele-specific expression and gene regulation help explain transgressive thermal tolerance in non-native hybrids of the endangered California tiger salamander (Ambystoma californiense). Mol. Ecol. 30, 987–1004 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Crow, J. C., Forstner, M. R. J., Ostr, K. G. & Tomasso, J. R. The role of temperature on survival and growth of the barton springs salamander (Eurycea sosorum). Herpetol. Conserv. Biol. 11, 328–334 (2016).
    Google Scholar 
    Cupp, P. V. Thermal tolerance of five salientian amphibians during development and metamorphosis. Herpetologica 36, 234–244 (1980).
    Google Scholar 
    Dabruzzi, T. F., Wygoda, M. L. & Bennett, W. A. Some like it hot: Heat tolerance of the crab-eating frog, Fejervarya cancrivora. Micronesica 43, 101–106 (2012).
    Google Scholar 
    Dainton, B. H. Heat tolerance and thyroid activity in developing tadpoles and juvenile adults of Xenopus laevis (Daudin). J. Therm. Biol. 16, 273–276 (1991).Article 

    Google Scholar 
    Daniel, N. J. J. Impact of climate change on Singapore amphibians. (National University of Singapore, 2013).Davies, S. J., McGeoch, M. A. & Clusella-Trullas, S. Plasticity of thermal tolerance and metabolism but not water loss in an invasive reed frog. Comp. Biochem. Physiol. 189, 11–20 (2015).CAS 
    Article 

    Google Scholar 
    de Oliviera Anderson, R. C., Bovo, R. P. & Andrade, D. V. Seasonal variation in the thermal biology of a terrestrial toad, Rhinella icterica (Bufonidae), from the Brazilian Atlantic Forest. J. Therm. Biol. 74, 77–83 (2018).Article 

    Google Scholar 
    de Vlaming, V. L. & Bury, R. B. Thermal selection in tadpoles of the tailed-frog. Ascaphus truei. J. Herpetol. 4, 179–189 (1970).Article 

    Google Scholar 
    Delson, J. & Whitford, W. G. Critical thermal maxima in several life history stages in desert and montane populations of Ambystoma tigrinum. Herpetologica 29, 352–355 (1973).
    Google Scholar 
    Duarte, H. et al. Can amphibians take the heat? Vulnerability to climate warming in subtropical and temperate larval amphibian communities. Glob. Chang. Biol. 18, 412–421 (2012).ADS 
    Article 

    Google Scholar 
    Duarte, H. S. A comparative study of the thermal tolerance of tadpoles of Iberian anurans. (Universidade de Lisboa, 2011).Dunlap, D. Evidence for a daily rhythm of heat resistance in cricket frogs, Acris crepitans. Copeia. 4, 852–854 (1969).Article 

    Google Scholar 
    Dunlap, D. G. Critical thermal maximum as a function of temperature of acclimation in two species of hylid frogs. Physiol. Zool. 41, 432–439 (1968).Article 

    Google Scholar 
    Elwood, J. R. L. Variation in hsp70 levels and thermotolerance among terrestrial salamanders of the Plethodon glutinosus complex. (Drexel University, 2003).Enriquez-Urzelai, U. et al. Ontogenetic reduction in thermal tolerance is not alleviated by earlier developmental acclimation in Rana temporaria. Oecologia 189, 385–394 (2019).ADS 
    PubMed 
    Article 

    Google Scholar 
    Enriquez-Urzelai, U. et al. The roles of acclimation and behaviour in buffering climate change impacts along elevational gradients. J. Anim. Ecol. 89, 1722–1734 (2020).PubMed 
    Article 

    Google Scholar 
    Erskine, D. J. & Hutchison, V. H. Reduced thermal tolerance in an amphibian treated with melatonin. J. Therm. Biol. 7, 121–123 (1982).CAS 
    Article 

    Google Scholar 
    Escobar Serrano, D. Acclimation scope of the critical thermal limits in Agalychnis spurrelli (Hylidae) and Gastrotheca pseustes (Hemiphractidae) and their implications under climate change scenarios. (Pontificia Universidad Católica Del Ecuador, 2016).Fan, X., Lei, H. & Lin, Z. Ontogenetic shifts in selected body temperature and thermal tolerance of the tiger frog. Hoplobatrachus chinensis. Acta Ecol. Sin. 32, 5574–5580 (2012).
    Google Scholar 
    Fan, X. L., Lin, Z. H. & Scheffers, B. R. Physiological, developmental, and behavioral plasticity in response to thermal acclimation. J. Therm. Biol. 97 (2021).Fernández-Loras, A. et al. Infection with Batrachochytrium dendrobatidis lowers heat tolerance of tadpole hosts and cannot be cleared by brief exposure to CTmax. PLoS ONE 14 (2019).Floyd, R. B. Ontogenetic change in the temperature tolerance of larval Bufo marinus (Anura: bufonidae). Comp. Biochem. Physiol. 75, 267–271 (1983).Article 

    Google Scholar 
    Floyd, R. B. Effects of photoperiod and starvation on the temperature tolerance of larvae of the giant toad, Bufo marinus. Copeia 1985, 625–631 (1985).MathSciNet 
    Article 

    Google Scholar 
    Fong, S.-T. Thermal tolerance of adult Asiatic painted frog Kaloula pulchra from different populations. (National University of Tainan, 2014).Frishkoff, L. O., Hadly, E. A. & Daily, G. C. Thermal niche predicts tolerance to habitat conversion in tropical amphibians and reptiles. Glob. Chang. Biol. 21, 3901–3916 (2015).ADS 
    PubMed 
    Article 

    Google Scholar 
    Frost, J. S. & Martin, E. W. A comparison of distribution and high temperature tolerance in Bufo americanus and Bufo woodhousii fowleri. Copeia 1971, 750 (1971).Article 

    Google Scholar 
    Gatz, A. J. Critical thermal maxima of Ambystoma maculatum (Shaw) and Ambystoma jeffersonianum (Green) in relation to time of breeding. Herpetologica 27, 157–160 (1971).
    Google Scholar 
    Gatz, A. J. Intraspecific variations in critical thermal maxima of Ambystoma maculatum. Herpetologica 29, 264–268 (1973).
    Google Scholar 
    Geise, W. & Linsenmair, K. E. Adaptations of the reed frog Hyperolius viridiflavus (Amphibia, Anura, Hyperoliidae) to its arid environment – IV. Ecological significance of water economy with comments on thermoregulation and energy allocation. Oecologia 77, 327–338 (1988).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    González-del-Pliego, P. et al. Thermal tolerance and the importance of microhabitats for Andean frogs in the context of land use and climate change. J. Anim. Ecol. 89, 2451–2460 (2020).PubMed 
    Article 

    Google Scholar 
    Gouveia, S. F. et al. Climatic niche at physiological and macroecological scales: The thermal tolerance-geographical range interface and niche dimensionality. Glob. Ecol. Biogeogr. 23, 446–456 (2014).Article 

    Google Scholar 
    Gray, R. Lack of physiological differentiation in three color morphs of the cricket frog (Acris crepitans) in Illinois. Trans. Ill. State Acad. Sci. 70, 73–79 (1977).ADS 

    Google Scholar 
    Greenspan, S. E. et al. Infection increases vulnerability to climate change via effects on host thermal tolerance. Sci. Rep. 7 (2017).Guevara-Molina, E. C., Gomes, F. R. & Camacho, A. Effects of dehydration on thermoregulatory behavior and thermal tolerance limits of Rana catesbeiana (Shaw, 1802). J. Therm. Biol. 93 (2020).Gutiérrez Pesquera, L. Una valoración macrofisiológica de la vulnerabilidad al calentamiento global. Análisis de los límites de tolerancia térmica en comunidades de anfibios en gradients latitudinales y altitudinales. (Pontificia Universidad Católica Del Ecuador, 2015).Gutiérrez Pesquera, M. Thermal tolerance across latitudinal and altitudinal gradients in tadpoles. (Universidad de Sevilla, 2016).Gutiérrez-Pesquera, L. M. et al. Testing the climate variability hypothesis in thermal tolerance limits of tropical and temperate tadpoles. J. Biogeogr. 43, 1166–1178 (2016).Article 

    Google Scholar 
    Gvoždík, L., Puky, M. & Šugerková, M. Acclimation is beneficial at extreme test temperatures in the Danube crested newt, Triturus dobrogicus (Caudata, Salamandridae). Bio. J. Linn. Soc. 90, 627–636 (2007).Article 

    Google Scholar 
    Heatwole, H., De Austin, S. B. & Herrero, R. Heat tolerances of tadpoles of two species of tropical anurans. Comp. Biochem. Physiol. 27, 807–815 (1968).Article 

    Google Scholar 
    Heatwole, H., Mercado, N. & Ortiz, E. Comparison of critical thermal maxima of two species of Puerto Rican frogs of the genus. Eleutherodactylus. Physiol. Zool. 38, 1–8 (1965).Article 

    Google Scholar 
    Holzman, N. & McManus, J. J. Effects of acclimation on metabolic rate and thermal tolerance in the carpenter frog. Rana vergatipes. Comp. Biochem. Physiol. 45, 833–842 (1973).CAS 
    Article 

    Google Scholar 
    Hoppe, D. M. Thermal tolerance in tadpoles of the chorus frog Pseudacris triseriata. Herpetologica 34, 318–321 (1978).
    Google Scholar 
    Hou, P.-C. Thermal tolerance and preference in the adult amphibians from different altitudinal LTER sites. (National Cheng Kung University, 2003).Howard, J. H., Wallace, R. L. & Stauffer, J. R. Jr Critical thermal maxima in populations of Ambystoma macrodactylum from different elevations. J. Herpetol. 17, 400–402 (1983).Article 

    Google Scholar 
    Hutchison, V. H. & Ritchart, J. P. Annual cycle of thermal tolerance in the salamander. Necturus maculosus. J. Herpetol. 23, 73–76 (1989).Article 

    Google Scholar 
    Hutchison, V. H. The distribution and ecology of the cave salamander, Eurycea lucifuga. Ecol. Monogr. 28, 2–20 (1958).Article 

    Google Scholar 
    Hutchison, V. H. Critical thermal maxima in salamanders. Physiol. Zool. 34, 92–125 (1961).Article 

    Google Scholar 
    Hutchison, V. H., Engbretson, G. & Turney, D. Thermal acclimation and tolerance in the hellbender, Cryptobranchus alleganiensis. Copeia 1973, 805–807 (1973).Article 

    Google Scholar 
    Hutchison, V. H. & Rowlan, S. D. Thermal acclimation and tolerance in the mudpuppy. Necturus maculosus. J. Herpetol. 9, 367–368 (1975).Article 

    Google Scholar 
    Jiang, S., Yu, P. & Hu, Q. A study on the critical thermal maxima of five species of salamanders of China. Acta Herpetol. Sin. 6, 56–62 (1987).
    Google Scholar 
    John-Alder, H. B., Morin, P. J. & Lawler, S. Thermal physiology, phenology, and distribution of tree frogs. Am. Nat. 132, 506–520 (1988).Article 

    Google Scholar 
    Johnson, C. R. Daily variation in the thermal tolerance of Litoria caerulea (Anura: Hylidae). Comp. Biochem. Physiol. 40, 1109–1111 (1971).Article 

    Google Scholar 
    Johnson, C. R. Thermal relations and water balance in the day frog, Taudactylus diurnus, from an Australian rain forest. Aust. J. Zool. 19, 35–39 (1971).Article 

    Google Scholar 
    Johnson, C. R. Diel variation in the thermal tolerance of Litoria gracilenta (Anura: Hylidae). Comp. Biochem. Physiol. 41, 727–730 (1972).CAS 
    Article 

    Google Scholar 
    Johnson, C. R. & Prine, J. E. The effects of sublethal concentrations of organophosphorus insecticides and an insect growth regulator on temperature tolerance in hydrated and dehydrated juvenile western toads. Bufo boreas. Comp. Biochem. Physiol. 53, 147–149 (1976).CAS 
    Article 

    Google Scholar 
    Johnson, C. R. Observations on body temperatures, critical thermal maxima and tolerance to water loss in the Australian hylid, Hyla caerulea (White). Proc. R. Soc. Qld. 82, 47–50 (1970).
    Google Scholar 
    Johnson, C. R. Thermal relations and daily variation in the thermal tolerance in. Bufo marinus. J. Herpetol. 6, 35 (1972).Article 

    Google Scholar 
    Johnson, C. Thermal relations in some southern and eastern Australian anurans. Proc. R. Soc. Qld. 82, 87–94 (1971).
    Google Scholar 
    Johnson, C. The effects of five organophosphorus insecticides on thermal stress in tadpoles of the Pacific tree frog. Hyla regilla. Zool. J. Linn. Soc. 69, 143–147 (1980).ADS 
    Article 

    Google Scholar 
    Katzenberger, M., Duarte, H., Relyea, R., Beltrán, J. F. & Tejedo, M. Variation in upper thermal tolerance among 19 species from temperate wetlands. J. Therm. Biol. 96 (2021).Katzenberger, M. et al. Swimming with predators and pesticides: How environmental stressors affect the thermal physiology of tadpoles. PLoS ONE 9 (2014).Katzenberger, M., Hammond, J., Tejedo, M. & Relyea, R. Source of environmental data and warming tolerance estimation in six species of North American larval anurans. J. Therm. Biol. 76, 171–178 (2018).PubMed 
    Article 

    Google Scholar 
    Katzenberger, M. Thermal tolerance and sensitivity of amphibian larvae from Palearctic and Neotropical communities. (Universidade de Lisboa, 2013).Katzenberger, M. Impact of global warming in holarctic and neotropical communities of amphibians. (Universidad de Sevilla, 2014).Kern, P., Cramp, R. L. & Franklin, C. E. Temperature and UV-B-insensitive performance in tadpoles of the ornate burrowing frog: An ephemeral pond specialist. J. Exp. Biol. 217, 1246–1252 (2014).PubMed 

    Google Scholar 
    Kern, P., Cramp, R. L., Seebacher, F., Ghanizadeh Kazerouni, E. & Franklin, C. E. Plasticity of protective mechanisms only partially explains interactive effects of temperature and UVR on upper thermal limits. Comp. Biochem. Physiol. 190, 75–82 (2015).CAS 
    Article 

    Google Scholar 
    Kern, P., Cramp, R. L. & Franklin, C. E. Physiological responses of ectotherms to daily temperature variation. J. Exp. Biol. 218, 3068–3076 (2015).PubMed 

    Google Scholar 
    Komaki, S., Igawa, T., Lin, S.-M. & Sumida, M. Salinity and thermal tolerance of Japanese stream tree frog (Buergeria japonica) tadpoles from island populations. Herpetol. J. 26, 207–211 (2016).
    Google Scholar 
    Komaki, S., Lau, Q. & Igawa, T. Living in a Japanese onsen: Field observations and physiological measurements of hot spring amphibian tadpoles. Buergeria japonica. Amphib. Reptil. 37, 311–314 (2016).Article 

    Google Scholar 
    Krakauer, T. Tolerance limits of the toad, Bufo marinus, in South Florida. Comp. Biochem. Physiol. 33, 15–26 (1970).CAS 
    PubMed 
    Article 

    Google Scholar 
    Kurabayashi, A. et al. Improved transport of the model amphibian, Xenopus tropicalis, and its viable temperature for transport. Curr. Herpetol. 33, 75–87 (2014).Article 

    Google Scholar 
    Lau, E. T. C., Leung, K. M. Y. & Karraker, N. E. Native amphibian larvae exhibit higher upper thermal limits but lower performance than their introduced predator. Gambusia affinis. J. Therm. Biol. 81, 154–161 (2019).PubMed 
    Article 

    Google Scholar 
    Layne, J. R. & Claussen, D. L. Seasonal variation in the thermal acclimation of critical thermal maxima (CTMax) and minima (CTMin) in the salamander. Eurycea bislineata. J. Therm. Biol. 7, 29–33 (1982).Article 

    Google Scholar 
    Layne, J. R. & Claussen, D. L. The time courses of CTMax and CTMin acclimation in the salamander. Desmognathus fuscus. J. Therm. Biol. 7, 139–141 (1982).Article 

    Google Scholar 
    Lee, P.-T. Acidic effect on tadpoles living in container habitats. (Tunghai University, 2019).Longhini, L. S., De Almeida Prado, C. P., Bícego, K. C., Zena, L. A. & Gargaglioni, L. H. Measuring cardiorespiratory variables on small tadpoles using a non-invasive methodology. Rev. Cuba. Investig. Biomed. 38 (2019).López Rosero, A. C. Ontogenetic variation of thermal tolerance in two anuran species of Ecuador: Gastrotheca pseustes (Hemiphractidae) and Smilisca phaeota (Hylidae) and their relative vulnerability to environmental temperature change. (Pontificia Universidad Católica Del Ecuador, 2015).Lotshaw, D. P. Temperature adaptation and effects of thermal acclimation in Rana sylvatica and Rana catesbeiana. Comp. Biochem. Physiol. 56, 287–294 (1977).Article 

    Google Scholar 
    Lu, H.-L., Wu, Q., Geng, J. & Dang, W. Swimming performance and thermal resistance of juvenile and adult newts acclimated to different temperatures. Acta Herpetol. 11, 189–195 (2016).
    Google Scholar 
    Lu, H. L., Geng, J., Xu, W., Ping, J. & Zhang, Y. P. Physiological response and changes in swimming performance after thermal acclimation in juvenile chinese fire-belly newts, Cynops orientalis. Acta Ecol. Sin. 37, 1603–1610 (2017).
    Google Scholar 
    Lutterschmidt, W. I. & Hutchison, V. H. The critical thermal maximum: Data to support the onset of spasms as the definitive end point. Can. J. Zool. 75, 1553–1560 (1997).Article 

    Google Scholar 
    Madalozzo, B. Variação latitudinal nos limites de tolerância e plasticidade térmica em anfíbios em um cenário de mudanças climáticas: efeito dos micro-habitats, sazonalidade e filogenia. (Universidade Federal de Santa Maria, 2018).Mahoney, J. J. & Hutchison, V. H. Photoperiod acclimation and 24-hour variations in the critical thermal maxima of a tropical and a temperate frog. Oecologia 2, 143–161 (1969).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Maness, J. D. & Hutchison, V. H. Acute adjustment of thermal tolerance in vertebrate ectotherms following exposure to critical thermal maxima. J. Therm. Biol. 5, 225–233 (1980).Article 

    Google Scholar 
    Manis, M. L. & Claussen, D. L. Environmental and genetic influences on the thermal physiology of Rana sylvatica. J. Therm. Biol. 11, 31–36 (1986).Article 

    Google Scholar 
    Markle, T. M. & Kozak, K. H. Low acclimation capacity of narrow-ranging thermal specialists exposes susceptibility to global climate change. Ecol. Evol. 8, 4644–4656 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Marshall, E. & Grigg, G. C. Acclimation of CTM, LD50, and rapid loss of acclimation of thermal preferendum in tadpoles of Limnodynastes peronii (Anura, Myobatrachidae). Aust. Zool. 20, 447–456 (1980).
    Google Scholar 
    Mathias, J. H. The Comparative ecologies of two species of Amphibia (B. bufo and B. calamita) on the Ainsdale Sand Dunes National Nature Reserve. (The University of Manchester, 1971).McManus, J. J. & Nellis, D. W. The critical thermal maximum of the marine toad, Bufo marinus. Caribb. J. Sci. 15, 67–70 (1975).
    Google Scholar 
    Menke, M. E. & Claussen, D. L. Thermal acclimation and hardening in tadpoles of the bullfrog, Rana catesbeiana. J. Therm. Biol. 7, 215–219 (1982).Article 

    Google Scholar 
    Merino-Viteri, A. R. The vulnerability of microhylid frogs, Cophixalus spp., to climate change in the Australian Wet Tropics. (James Cook University, 2018).Messerman, A. F. Tales of an ‘invisible’ life stage: Survival and physiology among terrestrial juvenile ambystomatid salamanders. (University of Missouri, 2019).Meza-Parral, Y., García-Robledo, C., Pineda, E., Escobar, F. & Donnelly, M. A. Standardized ethograms and a device for assessing amphibian thermal responses in a warming world. J. Therm. Biol. 89 (2020).Miller, K. & Packard, G. C. Critical thermal maximum: Ecotypic variation between montane and piedmont chorus frogs (Pseudacris triseriata, Hylidae). Experientia 30, 355–356 (1974).CAS 
    PubMed 
    Article 

    Google Scholar 
    Miller, K. & Packard, G. C. An altitudinal cline in critical thermal maxima of chorus frogs (Pseudacris triseriata). Am. Nat. 111, 267–277 (1977).Article 

    Google Scholar 
    Mueller, C. A., Bucsky, J., Korito, L. & Manzanares, S. Immediate and persistent effects of temperature on oxygen consumption and thermal tolerance in embryos and larvae of the baja California chorus frog, Pseudacris hypochondriaca. Front. Physiol. 10 (2019).Navas, C. A., Antoniazzi, M. M., Carvalho, J. E., Suzuki, H. & Jared, C. Physiological basis for diurnal activity in dispersing juvenile Bufo granulosus in the Caatinga, a Brazilian semi-arid environment. Comp. Biochem. Physiol. 147, 647–657 (2007).Article 

    Google Scholar 
    Navas, C. A., Úbeda, C. A., Logares, R. & Jara, F. G. Thermal tolerances in tadpoles of three species of Patagonian anurans. S. Am. J. Herpetol. 5, 89–96 (2010).Article 

    Google Scholar 
    Nietfeldt, J. W., Jones, S. M., Droge, D. L. & Ballinger, R. E. Rate of thermal acclimation of larval Ambystoma tigrinum. J. Herpetol. 14, 209–211 (1980).Article 

    Google Scholar 
    Nol, R. & Ultsch, G. R. The roles of temperature and dissolved oxygen in microhabitat selection by the tadpoles of a frog (Rana pipiens) and a toad (Bufo terrestris). Copeia 1981, 645–652 (1981).Article 

    Google Scholar 
    Novarro, A. J. Thermal physiology in a widespread lungless salamander. (University of Maryland, 2018).Nowakowski, A. J. et al. Thermal biology mediates responses of amphibians and reptiles to habitat modification. Ecol. Lett. 21, 345–355 (2018).PubMed 
    Article 

    Google Scholar 
    Orille, A. C., McWhinnie, R. B., Brady, S. P. & Raffel, T. R. Positive effects of acclimation temperature on the critical thermal maxima of Ambystoma mexicanum and Xenopus laevis. J. Herpetol. 54, 289–292 (2020).Article 

    Google Scholar 
    Oyamaguchi, H. M. et al. Thermal sensitivity of a neotropical amphibian (Engystomops pustulosus) and its vulnerability to climate change. Biotropica 50, 326–337 (2018).Article 

    Google Scholar 
    Paez Vacas, M. I. Mechanisms of population divergence along elevational gradients in the tropics. (Colorado State University, 2016).Paulson, B. K. & Hutchison, V. H. Blood changes in Bufo cognatus following acute heat stress. Comp. Biochem. Physiol. 87, 461–466 (1987).CAS 
    Article 

    Google Scholar 
    Paulson, B. & Hutchison, V. Origin of the stimulus for muscular spasms at the critical thermal maximum in anurans. Copeia 810–813 (1987).Percino-Daniel, R. et al. Environmental heterogeneity shapes physiological traits in tropical direct-developing frogs. Ecol. Evol. (2021).Perotti, M. G., Bonino, M. F., Ferraro, D. & Cruz, F. B. How sensitive are temperate tadpoles to climate change? The use of thermal physiology and niche model tools to assess vulnerability. Zoology 127, 95–105 (2018).PubMed 
    Article 

    Google Scholar 
    Pintanel, P., Tejedo, M., Almeida-Reinoso, F., Merino-Viteri, A. & Gutiérrez-Pesquera, L. M. Critical thermal limits do not vary between wild-caught and captive-bred tadpoles of Agalychnis spurrelli (Anura: Hylidae). Diversity 12, 43 (2020).Article 

    Google Scholar 
    Pintanel, P., Tejedo, M., Ron, S. R., Llorente, G. A. & Merino-Viteri, A. Elevational and microclimatic drivers of thermal tolerance in Andean Pristimantis frogs. J. Biogeogr. 46, 1664–1675 (2019).Article 

    Google Scholar 
    Pintanel, P. Thermal adaptation of amphibians in tropical mountains. Consequences of global warming. (Universitat de Barcelona, 2018).Pintanel, P., Tejedo, M., Salinas-Ivanenko, S., Jervis, P. & Merino-Viteri, A. Predators like it hot: Thermal mismatch in a predator-prey system across an elevational tropical gradient. J. Anim. Ecol. 90, 1985–1995 (2021).PubMed 
    Article 

    Google Scholar 
    Pough, F. H. Natural daily temperature acclimation of eastern red efts, Notophthalmus v. viridescens (Rafinesque) (Amphibia: Caudata). Comp. Biochem. Physiol. 47, 71–78 (1974).CAS 
    Article 

    Google Scholar 
    Pough, F. H., Stewart, M. M. & Thomas, R. G. Physiological basis of habitat partitioning in Jamaican. Eleutherodactylus. Oecologia 27, 285–293 (1977).ADS 
    PubMed 
    Article 

    Google Scholar 
    Quiroga, L. B., Sanabria, E. A., Fornés, M. W., Bustos, D. A. & Tejedo, M. Sublethal concentrations of chlorpyrifos induce changes in the thermal sensitivity and tolerance of anuran tadpoles in the toad Rhinella arenarum? Chemosphere 219, 671–677 (2019).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Rausch, C. The thermal ecology of the red-spotted toad, Bufo punctatus, across life history. (University of Nevada, 2007).Reichenbach, N. & Brophy, T. R. Natural history of the peaks of otter salamander (Plethodon hubrichti) along an elevational gradient. Herpetol. Bull. 141, 7–15 (2017).
    Google Scholar 
    Reider, K. E., Larson, D. J., Barnes, B. M. & Donnelly, M. A. Thermal adaptations to extreme freeze–thaw cycles in the high tropical Andes. Biotropica 53, 296–306 (2021).Article 

    Google Scholar 
    Richter-Boix, A. et al. Local divergence of thermal reaction norms among amphibian populations is affected by pond temperature variation. Evolution 69, 2210–2226 (2015).PubMed 
    Article 

    Google Scholar 
    Riquelme, N. A., Díaz-Páez, H. & Ortiz, J. C. Thermal tolerance in the Andean toad Rhinella spinulosa (Anura: Bufonidae) at three sites located along a latitudinal gradient in Chile. J. Therm. Biol. 60, 237–245 (2016).PubMed 
    Article 

    Google Scholar 
    Ritchart, J. P. & Hutchison, V. H. The effects of ATP and cAMP on the thermal tolerance of the mudpuppy. Necturus maculosus. J. Therm. Biol. 11, 47–51 (1986).CAS 
    Article 

    Google Scholar 
    Rivera-Burgos, A. C. Habitat suitability for Eleutherodactylus frogs in Puerto Rico: Indexing occupancy, abundance and reproduction to climatic and habitat characteristics. (North Carolina State University, 2019).Rivera-Ordonez, J. M., Nowakowski, A. J., Manansala, A., Thompson, M. E. & Todd, B. D. Thermal niche variation among individuals of the poison frog, Oophaga pumilio, in forest and converted habitats. Biotropica 51, 747–756 (2019).Article 

    Google Scholar 
    Romero Barreto, P. Requerimientos fisiológicos y microambientales de dos especies de anfibios (Scinax ruber e Hyloxalus yasuni) del bosque tropical de Yasuní y sus implicaciones ante el cambio climático. (Pontificia Universidad Católica Del Ecuador, 2013).Ruiz-Aravena, M. et al. Impact of global warming at the range margins: Phenotypic plasticity and behavioral thermoregulation will buffer an endemic amphibian. Ecol. Evol. 4, 4467–4475 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ruthsatz, K. et al. Thyroid hormone levels and temperature during development alter thermal tolerance and energetics of Xenopus laevis larvae. Conserv. Physiol. 6 (2018).Ruthsatz, K. et al. Post-metamorphic carry-over effects of altered thyroid hormone level and developmental temperature: physiological plasticity and body condition at two life stages in Rana temporaria. J. Comp. Physiol. B: Biochem. Syst. Environ. Physiol. 190, 297–315 (2020).CAS 
    Article 

    Google Scholar 
    Rutledge, P. S., Spotila, J. R. & Easton, D. P. Heat hardening in response to two types of heat shock in the lungless salamanders Eurycea bislineata and Desmognathus ochrophaeus. J. Therm. Biol. 12, 235–241 (1987).Article 

    Google Scholar 
    Sanabria, E. et al. Effect of salinity on locomotor performance and thermal extremes of metamorphic Andean Toads (Rhinella spinulosa) from Monte Desert, Argentina. J. Therm. Biol. 74, 195–200 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Sanabria, E. A., González, E., Quiroga, L. B. & Tejedo, M. Vulnerability to warming in a desert amphibian tadpole community: the role of interpopulational variation. J. Zool. 313, 283–296 (2021).Article 

    Google Scholar 
    Sanabria, E. A. & Quiroga, L. B. Change in the thermal biology of tadpoles of Odontophrynus occidentalis from the Monte desert, Argentina: Responses to photoperiod. J. Therm. Biol. 36, 288–291 (2011).Article 

    Google Scholar 
    Sanabria, E. A., Quiroga, L. B., González, E., Moreno, D. & Cataldo, A. Thermal parameters and locomotor performance in juvenile of Pleurodema nebulosum (Anura: Leptodactylidae) from the Monte Desert. J. Therm. Biol. 38, 390–395 (2013).Article 

    Google Scholar 
    Sanabria, E. A., Quiroga, L. B. & Martino, A. L. Seasonal changes in the thermal tolerances of the toad Rhinella arenarum (Bufonidae) in the Monte Desert of Argentina. J. Therm. Biol. 37, 409–412 (2012).Article 

    Google Scholar 
    Sanabria, E. A., Quiroga, L. B. & Martino, A. L. Seasonal Changes in the thermal tolerances of Odontophrynus occidentalis (Berg, 1896) (Anura: Cycloramphidae). Belg. J. Zool. 143, 23–29 (2013).
    Google Scholar 
    Sanabria, E. A. et al. Thermal ecology of the post-metamorphic Andean toad (Rhinella spinulosa) at elevation in the monte desert, Argentina. J. Therm. Biol. 52, 52–57 (2015).PubMed 
    Article 

    Google Scholar 
    Sanabria, E. A., Vaira, M., Quiroga, L. B., Akmentins, M. S. & Pereyra, L. C. Variation of thermal parameters in two different color morphs of a diurnal poison toad, Melanophryniscus rubriventris (Anura: Bufonidae). J. Therm. Biol. 41, 1–5 (2014).PubMed 
    Article 

    Google Scholar 
    Sanabria, E. A. & Quiroga, L. B. Thermal parameters changes in males of Rhinella arenarum (Anura: Bufonidae) related to reproductive periods. Rev. Biol. Trop. 59, 347–353 (2011).PubMed 

    Google Scholar 
    Scheffers, B. R. et al. Thermal buffering of microhabitats is a critical factor mediating warming vulnerability of frogs in the Philippine biodiversity hotspot. Biotropica 45, 628–635 (2013).Article 

    Google Scholar 
    Scheffers, B. R., Edwards, D. P., Diesmos, A., Williams, S. E. & Evans, T. A. Microhabitats reduce animal’s exposure to climate extremes. Glob. Chang. Biol. 20, 495–503 (2014).ADS 
    PubMed 
    Article 

    Google Scholar 
    Schmid, W. D. High temperature tolerances of Bufo Hemiophrys and Bufo Cognatus. Ecology 46, 559–560 (1965).Article 

    Google Scholar 
    Sealander, J. A. & West, B. W. Critical thermal maxima of some Arkansas salamanders in relation to thermal acclimation. Herpetologica 25, 122–124 (1969).
    Google Scholar 
    Seibel, R. V. Variables affecting the critical thermal maximum of the leopard frog, Rana pipiens Schreber. Herpetologica 26, 208–213 (1970).
    Google Scholar 
    Sherman, E. Ontogenetic change in thermal tolerance of the toad Bufo woodhousii fowleri. Comp. Biochem. Physiol. 65, 227–230 (1980).ADS 
    Article 

    Google Scholar 
    Sherman, E. Thermal biology of newts (Notophthalmus viridescens) chronically infected with a naturally occurring pathogen. J. Therm. Biol. 33, 27–31 (2008).Article 

    Google Scholar 
    Sherman, E., Baldwin, L., Fernandez, G. & Deurell, E. Fever and thermal tolerance in the toad Bufo marinus. J. Therm. Biol. 16, 297–301 (1991).Article 

    Google Scholar 
    Sherman, E. & Levitis, D. Heat hardening as a function of developmental stage in larval and juvenile Bufo americanus and Xenopus laevis. J. Therm. Biol. 28, 373–380 (2003).Article 

    Google Scholar 
    Shi, L., Zhao, L., Ma, X. & Ma, X. Selected body temperature and thermal tolerance of tadpoles of two frog species (Fejervarya limnocharis and Microhyla ornata) acclimated under different thermal conditions. Acta Ecol. Sin. 32, 0465–0471 (2012).Article 

    Google Scholar 
    Simon, M. N., Ribeiro, P. L. & Navas, C. A. Upper thermal tolerance plasticity in tropical amphibian species from contrasting habitats: Implications for warming impact prediction. J. Therm. Biol. 48, 36–44 (2015).PubMed 
    Article 

    Google Scholar 
    Simon, M. Plasticidade fenotípica em relação à temperatura de larvas de Rhinella (Anura: Bufonidae) da caatinga e da floresta Atlântica. (Universidade de Sao Paulo, 2010).Skelly, D. K. & Freidenburg, L. K. Effects of beaver on the thermal biology of an amphibian. Ecol. Lett. 3, 483–486 (2000).Article 

    Google Scholar 
    Sos, T. Thermoconformity even in hot small temporary water bodies: a case study in yellow-bellied toad (Bombina v. variegata). Herpetol. Rom. 1, 1–11 (2007).
    Google Scholar 
    Spotila, J. R. Role of temperature and water in the ecology of lungless salamanders. Ecol. Monogr. 42, 95–125 (1972).Article 

    Google Scholar 
    Tracy, C. R., Christian, K. A., Betts, G. & Tracy, C. R. Body temperature and resistance to evaporative water loss in tropical Australian frogs. Comp. Biochem. Physiol. 150, 102–108 (2008).Article 

    Google Scholar 
    Turriago, J. L., Parra, C. A. & Bernal, M. H. Upper thermal tolerance in anuran embryos and tadpoles at constant and variable peak temperatures. Can. J. Zool. 93, 267–272 (2015).Article 

    Google Scholar 
    Vidal, M. A., Novoa-Muñoz, F., Werner, E., Torres, C. & Nova, R. Modeling warming predicts a physiological threshold for the extinction of the living fossil frog Calyptocephalella gayi. J. Therm. Biol. 69, 110–117 (2017).PubMed 
    Article 

    Google Scholar 
    von May, R. et al. Divergence of thermal physiological traits in terrestrial breeding frogs along a tropical elevational gradient. Ecol. Evol. 7, 3257–3267 (2017).Article 

    Google Scholar 
    von May, R. et al. Thermal physiological traits in tropical lowland amphibians: Vulnerability to climate warming and cooling. PLoS ONE 14 (2019).Wagener, C., Kruger, N. & Measey, J. Progeny of Xenopus laevis from altitudinal extremes display adaptive physiological performance. J. Exp. Biol. 224 (2021).Wang, H. & Wang, L. Thermal adaptation of the common giant toad (Bufo gargarizans) at different earlier developmental stages. J. Agric. Univ. Hebei 31, 79–83 (2008).
    Google Scholar 
    Wang, L. The effects of constant and variable thermal acclimation on thermal tolerance of the common giant toad tadpoles (Bufo gargarizans). Acta Ecol. Sin. 34, 1030–1034 (2014).
    Google Scholar 
    Wang, L.-Z. & Li, X.-C. Effect of temperature on incubation and thermal tolerance of the Chinese forest frog. Chin. J. Zool. (2007).Wang, L. & Li, X.-C. Effects of constant thermal acclimation on thermal tolerance of the Chinese forest frog (Rana chensineniss). Acta Hydrobiol. Sin. 31, 748–750 (2007).CAS 

    Google Scholar 
    Wang, L.-Z., Li, X.-C. & Sun, T. Preferred temperature, avoidance temperature and lethal temperature of tadpoles of the common giant toad (Bufo gargarizans) and the Chinese forest frog (Rana chensinensis). Chin. J. Zool. 40, 23–27 (2005).
    Google Scholar 
    Warburg, M. R. On the water economy of Israel amphibians: The anurans. Comp. Biochem. Physiol. 40, 911–924 (1971).CAS 
    Article 

    Google Scholar 
    Warburg, M. R. The water economy of Israel amphibians: The urodeles Triturus vittatus (Jenyns) and Salamandra salamandra (L.). Comp. Biochem. Physiol. 40, 1055–1056, IN11,1057–1063 (1971).Willhite, C. & Cupp, P. V. Daily rhythms of thermal tolerance in Rana clamitans (Anura: Ranidae) tadpoles. Comp. Biochem. Physiol. 72, 255–257 (1982).Article 

    Google Scholar 
    Wu, C.-S. & Kam, Y.-C. Thermal tolerance and thermoregulation by Taiwanese rhacophorid tadpoles (Buergeria japonica) living in geothermal hot springs and streams. Herpetologica 61, 35–46 (2005).Article 

    Google Scholar 
    Xu, X. The effect of temperature on body temperature and thermoregulation in different geographic populations of Rana dybowskii. (Harbin Normal University, 2017).Yandún Vela, M. C. Capacidad de aclimatación en renacuajos de dos especies de anuros: Rhinella marina (Bufonidae) y Gastrotheca riobambae (Hemiphractidae) y su vulnerabilidad al cambio climático. (Pontificia Universidad Católica Del Ecuador, 2017).Young, V. K. H. & Gifford, M. E. Limited capacity for acclimation of thermal physiology in a salamander. Desmognathus brimleyorum. J. Comp. Physiol. B: Biochem. Syst. Environ. Physiol. 183, 409–418 (2013).CAS 
    Article 

    Google Scholar 
    Yu, Z., Dickstein, R., Magee, W. E. & Spotila, J. R. Heat shock response in the salamanders Plethodon jordani and Plethodon cinereus. J. Therm. Biol. 23, 259–265 (1998).CAS 
    Article 

    Google Scholar 
    Zheng, R.-Q. & Liu, C.-T. Giant spiny-frog (Paa spinosa) from different populations differ in thermal preference but not in thermal tolerance. Aquat. Ecol. 44, 723–729 (2010).Article 

    Google Scholar 
    Zweifel, R. G. Studies on the critical thermal maxima of salamanders. Ecology 38, 64–69 (1957).Article 

    Google Scholar 
    Pick, J. L., Nakagawa, S. & Noble, D. W. A. Reproducible, flexible and high-throughput data extraction from primary literature: The metaDigitise r package. Methods Ecol. Evol. 10, 426–431 (2019).Article 

    Google Scholar 
    R Core Team. R: A language and environment for statistical computing.Jetz, W. & Pyron, R. A. The interplay of past diversification and evolutionary isolation with present imperilment across the amphibian tree of life. Nat. Ecol. Evol. 2, 850–858 (2018).PubMed 
    Article 

    Google Scholar 
    AmphibiaWeb. https://amphibiaweb.org. University of California, Berkeley, California, USA (2022).Schwanz, L. E. et al. Best practices for building and curating databases for comparative analyses. J. Exp. Biol. 225, jeb243295 (2022).PubMed 
    Article 

    Google Scholar 
    Pottier, P. et al. A comprehensive database of amphibian heat tolerance, Zenodo, https://doi.org/10.5281/zenodo.6565454 (2022).Lajeunesse, M. J. Recovering Missing or Partial Data from Studies: A Survey of Conversions and Imputations for Meta-analysis. in Hanbook of Meta-analysis in Ecology and Evolution 195–206 (Princeton University Press, 2013).Nakagawa, S., et al. A robust and readily implementable method for the meta-analysis of response ratios with and without missing standard deviations. EcoEvoRxiv, https://doi.org/10.32942/osf.io/7thx9 (2022)Pottier, P., Burke, S., Drobniak, S. M., Lagisz, M. & Nakagawa, S. Sexual (in)equality? A meta-analysis of sex differences in thermal acclimation capacity across ectotherms. Funct. Ecol. 35, 2663–2678 (2021).Article 

    Google Scholar 
    Sunday, J. et al. Thermal tolerance patterns across latitude and elevation. Philos. Trans. R. Soc. B-Biol. Sci. 374, 20190036 (2019).Article 

    Google Scholar 
    Truebano, M., Fenner, P., Tills, O., Rundle, S. D. & Rezende, E. L. Thermal strategies vary with life history stage. J. Exp. Biol. 221, jeb171629 (2018).PubMed 
    Article 

    Google Scholar 
    Rezende, E. L., Tejedo, M. & Santos, M. Estimating the adaptive potential of critical thermal limits: methodological problems and evolutionary implications. Funct. Ecol. 25, 111–121 (2011).Article 

    Google Scholar 
    Terblanche, J. S., Deere, J. A., Clusella-Trullas, S., Janion, C. & Chown, S. L. Critical thermal limits depend on methodological context. Proc. R. Soc. B-Biol. Sci. 274, 2935–2943 (2007).Article 

    Google Scholar 
    Hangartner, S., Sgrò, C. M., Connallon, T. & Booksmythe, I. Sexual dimorphism in phenotypic plasticity and persistence under environmental change: An extension of theory and meta-analysis of current data. Ecol. Lett. (2022).Wickham, H. et al. Welcome to the tidyverse. J. Open Source Softw. 4, 1686 (2019).ADS 
    Article 

    Google Scholar 
    Dunnington, D. & Thorne, B. ggspatial: Spatial Data Framework for ggplot2. R package (2020).Brownrigg, M. R. Package ‘maps’. R package (2013).Yu, G., Smith, D. K., Zhu, H., Guan, Y. & Lam, T. T.-Y. ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol. Evol. 8, 28–36 (2017).Article 

    Google Scholar 
    Xu, S. et al. ggtreeExtra: Compact visualization of richly annotated phylogenetic data. Mol. Biol. Evol. 38, 4039–4042 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Campitelli, E. ggnewscale: Multiple fill and colour scales in “ggplot2”. R package (2020).Pedersen, T. L. patchwork: The Composer of Plots. R package (2020).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  More

  • in

    Spatial coalescent connectivity through multi-generation dispersal modelling predicts gene flow across marine phyla

    Hellberg, M. E. Gene flow and isolation among populations of marine animals. Annu. Rev. Ecol. Evol. Syst. 40, 291–310 (2009).
    Google Scholar 
    Lenormand, T. Gene flow and the limits to natural selection. Trends Ecol. Evol. 17, 183–189 (2002).
    Google Scholar 
    Lowe, W. H., Kovach, R. P. & Allendorf, F. W. Population genetics and demography unite ecology and evolution. Trends Ecol. Evol. 32, 141–152 (2017).PubMed 

    Google Scholar 
    Slatkin, M. Gene flow and the geographic structure of natural populations. Science 236, 787–792 (1987).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Slatkin, M. Gene flow in natural populations. Annu. Rev. Ecol. Syst. 1, 393–430 (1985).
    Google Scholar 
    Duputié, A. & Massol, F. An empiricist’s guide to theoretical predictions on the evolution of dispersal. Interface Focus 3, 20130028 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    Lowe, W. H. & Allendorf, F. W. What can genetics tell us about population connectivity? Mol. Ecol. 19, 3038–3051 (2010).PubMed 

    Google Scholar 
    Selkoe, K. A. et al. A decade of seascape genetics: contributions to basic and applied marine connectivity. Mar. Ecol. Prog. Ser. 554, 1–19 (2016).ADS 

    Google Scholar 
    Weersing, K. & Toonen, R. J. Population genetics, larval dispersal, and connectivity in marine systems. Mar. Ecol. Prog. Ser. 393, 1–12 (2009).ADS 

    Google Scholar 
    Whitlock, M. C. & Mccauley, D. E. Indirect measures of gene flow and migration: FST≠1/(4Nm+1). Heredity 82, 117–125 (1999).PubMed 

    Google Scholar 
    Benestan, L. et al. Restricted dispersal in a sea of gene flow. Proc. R. Soc. B Biol. Sci. 288, 20210458 (2021).CAS 

    Google Scholar 
    Bode, M. et al. Successful validation of a larval dispersal model using genetic parentage data. PLoS Biol. 17, e3000380 (2019).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gagnaire, P.-A. Comparative genomics approach to evolutionary process connectivity. Evol. Appl. 13, 1320–1334 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    Pinsky, M. L. et al. Marine dispersal scales are congruent over evolutionary and ecological time. Curr. Biol. 27, 149–154 (2017).CAS 
    PubMed 

    Google Scholar 
    Baguette, M., Blanchet, S., Legrand, D., Stevens, V. M. & Turlure, C. Individual dispersal, landscape connectivity and ecological networks. Biol. Rev. 88, 310–326 (2013).PubMed 

    Google Scholar 
    Cowen, R. K. & Sponaugle, S. Larval dispersal and marine population connectivity. Annu. Rev. Mar. Sci. 1, 443–466 (2009).ADS 

    Google Scholar 
    Tomback, D. F., Anderies, A. J., Carsey, K. S., Powell, M. L. & Mellmann-Brown, S. Delayed seed germination in whitebark pine and regeneration patterns following the yellowstone fires. Ecology 82, 2587–2600 (2001).
    Google Scholar 
    Viana, D. S., Santamaría, L. & Figuerola, J. Migratory birds as global dispersal vectors. Trends Ecol. Evol. 31, 763–775 (2016).PubMed 

    Google Scholar 
    Nathan, R. et al. Mechanisms of long-distance dispersal of seeds by wind. Nature 418, 409–413 (2002).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Cowen, R. K., Paris, C. B. & Srinivasan, A. Scaling of connectivity in marine populations. Science 311, 522–527 (2006).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Shanks, A. L. Pelagic larval duration and dispersal distance revisited. Biol. Bull. 216, 373–385 (2009).PubMed 

    Google Scholar 
    Hidalgo, M. et al. Accounting for ocean connectivity and hydroclimate in fish recruitment fluctuations within transboundary metapopulations. Ecol. Appl. 29, e01913 (2019).Legrand, T., Di Franco, A., Ser-Giacomi, E., Caló, A. & Rossi, V. A multidisciplinary analytical framework to delineate spawning areas and quantify larval dispersal in coastal fish. Mar. Environ. Res. 151, 104761 (2019).CAS 
    PubMed 

    Google Scholar 
    Blowes, S. A. et al. The geography of biodiversity change in marine and terrestrial assemblages. Science 366, 339–345 (2019).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Marshall, D. J., Monro, K., Bode, M., Keough, M. J. & Swearer, S. Phenotype–environment mismatches reduce connectivity in the sea. Ecol. Lett. 13, 128–140 (2010).CAS 
    PubMed 

    Google Scholar 
    Crandall, E. D., Treml, E. A. & Barber, P. H. Coalescent and biophysical models of stepping-stone gene flow in neritid snails. Mol. Ecol. 21, 5579–5598 (2012).PubMed 

    Google Scholar 
    Smith, T. M. et al. Rare long-distance dispersal of a marine angiosperm across the Pacific Ocean. Glob. Ecol. Biogeogr. 27, 487–496 (2018).
    Google Scholar 
    Saura, S., Bodin, Ö. & Fortin, M.-J. EDITOR’S CHOICE: Stepping stones are crucial for species’ long‐distance dispersal and range expansion through habitat networks. J. Appl. Ecol. 51, 171–182 (2014).
    Google Scholar 
    Lett, C., Barrier, N. & Bahlali, M. Converging approaches for modeling the dispersal of propagules in air and sea. Ecol. Model. 415, 108858 (2020).
    Google Scholar 
    D’Aloia, C. C. et al. Patterns, causes, and consequences of marine larval dispersal. Proc. Natl Acad. Sci. USA 112, 13940–13945 (2015).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kool, J. T., Moilanen, A. & Treml, E. A. Population connectivity: recent advances and new perspectives. Landsc. Ecol. 28, 165–185 (2013).
    Google Scholar 
    Mari, L., Melià, P., Fraschetti, S., Gatto, M. & Casagrandi, R. Spatial patterns and temporal variability of seagrass connectivity in the Mediterranean Sea. Divers. Distrib. 26, 169–182 (2020).
    Google Scholar 
    Nathan, R., Klein, E. K., Robledo-Arnuncio, J. J. & Revilla, E. Dispersal Kernels. vol. 15 (Oxford University Press Oxford, UK, 2012).Boulanger, E., Dalongeville, A., Andrello, M., Mouillot, D. & Manel, S. Spatial graphs highlight how multi-generational dispersal shapes landscape genetic patterns. Ecography 43, 1167–1179 (2020).
    Google Scholar 
    Jahnke, M. et al. Seascape genetics and biophysical connectivity modelling support conservation of the seagrass Zostera marina in the Skagerrak–Kattegat region of the eastern North Sea. Evol. Appl. 11, 645–661 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    Jahnke, M. & Jonsson, P. R. Biophysical models of dispersal contribute to seascape genetic analyses. Philos. Trans. R. Soc. B Biol. Sci. 377, 20210024 (2022).
    Google Scholar 
    Buonomo, R. et al. Habitat continuity and stepping-stone oceanographic distances explain population genetic connectivity of the brown alga Cystoseira amentacea. Mol. Ecol. 26, 766–780 (2017).PubMed 

    Google Scholar 
    Assis, J. et al. Ocean currents shape the genetic structure of a kelp in southwestern Africa. J. Biogeogr. 49, 822–835 (2022).
    Google Scholar 
    Ser-Giacomi, E., Vasile, R., Hernández-García, E. & López, C. Most probable paths in temporal weighted networks: An application to ocean transport. Phys. Rev. E 92, 012818 (2015).ADS 

    Google Scholar 
    McRae, B. H. & Beier, P. Circuit theory predicts gene flow in plant and animal populations. Proc. Natl Acad. Sci. USA 104, 19885–19890 (2007).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Foster, N. L. et al. Connectivity of Caribbean coral populations: complementary insights from empirical and modelled gene flow. Mol. Ecol. 21, 1143–1157 (2012).PubMed 

    Google Scholar 
    Kool, J. T., Paris, C. B., Andréfouët, S. & Cowen, R. K. Complex migration and the development of genetic structure in subdivided populations: an example from Caribbean coral reef ecosystems. Ecography 33, 597–606 (2010).
    Google Scholar 
    White, J. W., Botsford, L. W., Hastings, A. & Largier, J. L. Population persistence in marine reserve networks: incorporating spatial heterogeneities in larval dispersal. Mar. Ecol. Prog. Ser. 398, 49–67 (2010).ADS 

    Google Scholar 
    Ser-Giacomi, E., Legrand, T., Hernández-Carrasco, I. & Rossi, V. Explicit and implicit network connectivity: Analytical formulation and application to transport processes. Phys. Rev. E 103, 042309 (2021).ADS 
    MathSciNet 
    CAS 
    PubMed 

    Google Scholar 
    Battiston, F. et al. Networks beyond pairwise interactions: structure and dynamics. Phys. Rep. 874, 1–92 (2020).ADS 
    MathSciNet 
    MATH 

    Google Scholar 
    Levine, J. M., Bascompte, J., Adler, P. B. & Allesina, S. Beyond pairwise mechanisms of species coexistence in complex communities. Nature 546, 56–64 (2017).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Mayfield, M. M. & Stouffer, D. B. Higher-order interactions capture unexplained complexity in diverse communities. Nat. Ecol. Evol. 1, 1–7 (2017).
    Google Scholar 
    Rousset, F. Inferences from spatial population genetics. Handb. Stat. Genet. 4, 23 (2001).
    Google Scholar 
    Dubois, M. et al. Linking basin-scale connectivity, oceanography and population dynamics for the conservation and management of marine ecosystems. Glob. Ecol. Biogeogr. 25, 503–515 (2016).
    Google Scholar 
    Monroy, P., Rossi, V., Ser-Giacomi, E., López, C. & Hernández-García, E. Sensitivity and robustness of larval connectivity diagnostics obtained from Lagrangian Flow Networks. ICES J. Mar. Sci. 74, 1763–1779 (2017).
    Google Scholar 
    Rossi, V., Ser-Giacomi, E., López, C. & Hernández-García, E. Hydrodynamic provinces and oceanic connectivity from a transport network help designing marine reserves. Geophys. Res. Lett. 41, 2883–2891 (2014).ADS 

    Google Scholar 
    Ser-Giacomi, E., Rossi, V., Lopez, C. & Hernandez-Garcia, E. Flow networks: A characterization of geophysical fluid transport. Chaos Interdiscip. J. Nonlinear Sci. 25, 036404 (2015).
    Google Scholar 
    Oddo, P. et al. A nested Atlantic-Mediterranean Sea general circulation model for operational forecasting. Ocean Sci. 5, 461–473 (2009).Rousset, F. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145, 1219–1228 (1997).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Reem, E., Douek, J., Paz, G., Katzir, G. & Rinkevich, B. Phylogenetics, biogeography and population genetics of the ascidian Botryllus schlosseri in the Mediterranean Sea and beyond. Mol. Phylogenet. Evol. 107, 221–231 (2017).PubMed 

    Google Scholar 
    Villamor, A., Costantini, F. & Abbiati, M. Genetic structuring across marine biogeographic boundaries in rocky shore invertebrates. PLoS ONE 9, e101135 (2014).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Borrero-Pérez, G. H., González-Wangüemert, M., Marcos, C. & Pérez-Ruzafa, A. Phylogeography of the Atlanto-Mediterranean sea cucumber Holothuria (Holothuria) mammata: the combined effects of historical processes and current oceanographical pattern: PHYLOGEOGRAPHY OF HOLOTHURIA MAMMATA. Mol. Ecol. 20, 1964–1975 (2011).PubMed 

    Google Scholar 
    Carreras, C. et al. East is East and West is West: Population genomics and hierarchical analyses reveal genetic structure and adaptation footprints in the keystone species Paracentrotus lividus (Echinoidea). Divers. Distrib. 26, 382–398 (2020).
    Google Scholar 
    Aurelle, D. et al. Phylogeography of the red coral (Corallium rubrum): inferences on the evolutionary history of a temperate gorgonian. Genetica 139, 855–869 (2011).CAS 
    PubMed 

    Google Scholar 
    Costantini, F., Carlesi, L. & Abbiati, M. Quantifying spatial genetic structuring in mesophotic populations of the precious coral Corallium rubrum. PLoS ONE 8, e61546 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Durand, J., Blel, H., Shen, K., Koutrakis, E. & Guinand, B. Population genetic structure of Mugil cephalus in the Mediterranean and Black Seas: a single mitochondrial clade and many nuclear barriers. Mar. Ecol. Prog. Ser. 474, 243–261 (2013).ADS 

    Google Scholar 
    Alberto, F. et al. Genetic differentiation and secondary contact zone in the seagrass Cymodocea nodosa across the Mediterranean–Atlantic transition region. J. Biogeogr. 35, 1279–1294 (2008).
    Google Scholar 
    McRae, B. H. Isolation by resistance. Evolution 60, 1551–1561 (2006).PubMed 

    Google Scholar 
    Dalongeville, A. et al. Geographic isolation and larval dispersal shape seascape genetic patterns differently according to spatial scale. Evol. Appl. 11, 1437–1447 (2018).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Jenkins, D. G. et al. A meta‐analysis of isolation by distance: relic or reference standard for landscape genetics? Ecography 33, 315–320 (2010).
    Google Scholar 
    Selkoe, K. A. & Toonen, R. J. Marine connectivity: a new look at pelagic larval duration and genetic metrics of dispersal. Mar. Ecol. Prog. Ser. 436, 291–305 (2011).ADS 

    Google Scholar 
    Alberto, F. et al. Isolation by oceanographic distance explains genetic structure for Macrocystis pyrifera in the Santa Barbara Channel. Mol. Ecol. 20, 2543–2554 (2011).PubMed 

    Google Scholar 
    Selkoe, K. A. et al. Taking the chaos out of genetic patchiness: seascape genetics reveals ecological and oceanographic drivers of genetic patterns in three temperate reef species. Mol. Ecol. 19, 3708–3726 (2010).PubMed 

    Google Scholar 
    Xuereb, A. et al. Asymmetric oceanographic processes mediate connectivity and population genetic structure, as revealed by RADseq, in a highly dispersive marine invertebrate (Parastichopus californicus). Mol. Ecol. 27, 2347–2364 (2018).PubMed 

    Google Scholar 
    Pascual, M., Rives, B., Schunter, C. & Macpherson, E. Impact of life history traits on gene flow: A multispecies systematic review across oceanographic barriers in the Mediterranean Sea. PLoS ONE 12, e0176419 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Wang, I. J., Glor, R. E. & Losos, J. B. Quantifying the roles of ecology and geography in spatial genetic divergence. Ecol. Lett. 16, 175–182 (2013).PubMed 

    Google Scholar 
    Bierne, N., Welch, J., Loire, E., Bonhomme, F. & David, P. The coupling hypothesis: why genome scans may fail to map local adaptation genes. Mol. Ecol. 20, 2044–2072 (2011).PubMed 

    Google Scholar 
    Sen Gupta, A. et al. Future changes to the upper ocean Western Boundary Currents across two generations of climate models. Sci. Rep. 11, 9538 (2021).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ser-Giacomi, E. et al. Impact of climate change on surface stirring and transport in the Mediterranean Sea. Geophys. Res. Lett. 47, e2020GL089941 (2020).ADS 
    CAS 

    Google Scholar 
    Jorda, G. et al. Ocean warming compresses the three-dimensional habitat of marine life. Nat. Ecol. Evol. 4, 109–114 (2020).PubMed 

    Google Scholar 
    Wright, S. Evolution in mendelian populations. Genetics 16, 97–159 (1931).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Eldon, B., Riquet, F., Yearsley, J., Jollivet, D. & Broquet, T. Current hypotheses to explain genetic chaos under the sea. Curr. Zool. 62, 551–566 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Schunter, C. et al. A novel integrative approach elucidates fine-scale dispersal patchiness in marine populations. Sci. Rep. 9, 1–10 (2019).ADS 
    CAS 

    Google Scholar 
    Jackson, T. M., Roegner, G. C. & O’Malley, K. G. Evidence for interannual variation in genetic structure of Dungeness crab (Cancer magister) along the California Current System. Mol. Ecol. 27, 352–368 (2018).CAS 
    PubMed 

    Google Scholar 
    Pascual, M. et al. Temporal and spatial genetic differentiation in the crab Liocarcinus depurator across the Atlantic-Mediterranean transition. Sci. Rep. 6, 29892 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Pérez-Portela, R. et al. Spatio-temporal patterns of genetic variation in Arbacia lixula, a thermophilous sea urchin in expansion in the Mediterranean. Heredity 122, 244–259 (2019).PubMed 

    Google Scholar 
    Carroll, S. P., Hendry, A. P., Reznick, D. N. & Fox, C. W. Evolution on ecological time-scales. Funct. Ecol. 21, 387–393 (2007).
    Google Scholar 
    Grilli, J., Barabás, G., Michalska-Smith, M. J. & Allesina, S. Higher-order interactions stabilize dynamics in competitive network models. Nature 548, 210–213 (2017).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Butchart, S. H. M. et al. Global biodiversity: indicators of recent declines. Science 328, 1164–1168 (2010).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Sala, E. et al. Protecting the global ocean for biodiversity, food and climate. Nature 592, 397–402 (2021).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Hauser, L. & Carvalho, G. R. Paradigm shifts in marine fisheries genetics: ugly hypotheses slain by beautiful facts. Fish. Fish. 9, 333–362 (2008).
    Google Scholar 
    Weber, A. A.-T., Mérigot, B., Valière, S. & Chenuil, A. Influence of the larval phase on connectivity: strong differences in the genetic structure of brooders and broadcasters in the Ophioderma longicauda species complex. Mol. Ecol. 24, 6080–6094 (2015).CAS 
    PubMed 

    Google Scholar 
    Marzouk, Z., Aurelle, D., Said, K. & Chenuil, A. Cryptic lineages and high population genetic structure in the exploited marine snail Hexaplex trunculus (Gastropoda: Muricidae). Biol. J. Linn. Soc. 122, 411–428 (2017).
    Google Scholar 
    Cowen, R. K., Lwiza, K. M., Sponaugle, S., Paris, C. B. & Olson, D. B. Connectivity of marine populations: open or closed? Science 287, 857–859 (2000).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Pante, E. & Simon-Bouhet, B. marmap: a package for importing, plotting and analyzing bathymetric and topographic data in R. PLoS ONE 8, e73051 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Susini, M.-L., Thibaut, T., Meinesz, A. & Forcioli, D. A preliminary study of genetic diversity in Cystoseira amentacea (C. Agardh) Bory var. stricta Montagne (Fucales, Phaeophyceae) using random amplified polymorphic DNA. Phycologia 46, 605–611 (2007).
    Google Scholar  More

  • in

    Saltwater intrusion indirectly intensifies Phragmites australis invasion via alteration of soil microbes

    Dookes, J. S. & Mooney, H. A. Does global change increase the success of biological invaders?. Trends Ecol. Evol. 14, 135–139 (1999).Article 

    Google Scholar 
    Gallien, L. & Carboni, M. The community ecology of invasive species: Where are we and what’s next?. Ecography 40, 335–352 (2017).Article 

    Google Scholar 
    Tylianakis, J. M., Didham, R. K., Bascompte, J. & Wardle, D. A. Global change and species interactions in terrestrial ecosystems. Ecol. Lett. 11, 1351–1363 (2008).PubMed 
    Article 

    Google Scholar 
    Adler, P. B., Dalgleish, H. J. & Ellner, S. P. Forecasting plant community impacts of climate variability and change: When do competitive interactions matter?. J. Ecol. 100, 478–487 (2012).Article 

    Google Scholar 
    Cahill, A. E., Aiello-Lammens, M. E., Fisher-Reid, M. C. & Hua, X. How does climate change cause extinction?. Proc. Biol. Sci. 280, 20121890 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    Ockendon, N. et al. Mechanisms underpinning climatic impacts on natural populations: Altered species interactions are more important than direct effects. Glob. Chang. Biol. 20, 2221–2229 (2014).ADS 
    PubMed 
    Article 

    Google Scholar 
    Chu, C. et al. Direct effects dominate responses to climate perturbations in grassland plant communities. Nat. Commun. 7, 11766 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Gunderson, A. R., Tsukimura, B. & Stillman, J. H. Indirect effects of global change: From physiological and behavioral mechanisms to ecological consequences. Integr. Comp. Biol. 57, 48–54 (2017).PubMed 
    Article 

    Google Scholar 
    Suttle, K. B., Thomsen, M. A. & Power, M. E. Species interactions reverse grassland responses to changing climate. Science 315, 640–642 (2007).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Farrer, E. C. et al. Indirect effects of global change accumulate to alter plant diversity but not ecosystem function in alpine tundra. J. Ecol. 103, 351–360 (2015).CAS 
    Article 

    Google Scholar 
    Sentis, A., Montoya, J. M. & Lurgi, M. Warming indirectly increases invasion success in food webs. Proc. R. Soc. B. 288, 1947 (2021).Article 

    Google Scholar 
    Ohgushi, T. Indirect interaction webs: Herbivore-induced effects through trait change in plants. Annu. Rev. Ecol. Evol. Syst. 36, 81–105 (2005).Article 

    Google Scholar 
    Classen, A. et al. Direct and indirect effects of climate change on soil microbial and soil microbial-plant interactions: What lies ahead?. Ecosphere 6, 1–21 (2015).Article 

    Google Scholar 
    Van-der-Putten, W. H., Macel, M. & Visser, M. E. Predicting species distributions and abundance responses to climate change: Why it is essential to include biotic interactions across trophic levels. Philos. Trans. R. Soc. B. 365, 2025–2034 (2010).Article 

    Google Scholar 
    Rudgers, J. A. et al. Climate disruption of plant-microbe interactions. Annu. Rev. Ecol. Evol. Syst. 51, 561–586 (2020).Article 

    Google Scholar 
    Deltedesco, E. et al. Soil microbial community structure and function mainly respond to indirect effects in a multifactorial climate manipulation experiment. Soil Biol. Biochem. 142, 1–12 (2020).Article 

    Google Scholar 
    Fahey, C., Koyama, A., Antunes, P. M., Dunfield, K. & Flory, S. L. Plant communities mediate the interactive effects of invasion and drought on soil microbial communities. ISME 14, 1396–1409 (2020).Article 

    Google Scholar 
    Nuccio, E. E. et al. An arbuscular mycorrhizal fungus significantly modifies the soil bacterial community and nitrogen cycling during litter decomposition. Environ. Microbiol. 15, 1870–1881 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bennett, J. A. & Cahill, J. F. Fungal effects on plant–plant interactions contribute to grassland plant abundances: Evidence from the field. J. Ecol. 104, 755–764 (2016).Article 

    Google Scholar 
    Reinhart, K. O. & Callaway, R. M. Soil biota and invasive plants. New Phytol. 170, 445–457 (2006).PubMed 
    Article 

    Google Scholar 
    Inderjit, C. J. F. Linkages of plant–soil feedbacks and underlying invasion mechanisms. AoB Plants 7, 1–8 (2015).CAS 
    Article 

    Google Scholar 
    Lekberg, Y. et al. Relative importance of competition and plant–soil feedback, their synergy, context dependency and implications for coexistence. Ecol. Lett. 21, 1268–1281 (2018).PubMed 
    Article 

    Google Scholar 
    Teh, S. Y. & Koh, H. L. Climate change and soil salinization: Impact on agriculture, water, and food security. IJAFP 2, 1–9 (2016).
    Google Scholar 
    White, E. Restore or retreat? Saltwater intrusion and coastal management in coastal wetlands. Ecosyst. Health Sustain. https://doi.org/10.1002/ehs2.1258 (2016).Article 

    Google Scholar 
    Donnolly, J. P. & Bertness, M. D. Rapid shoreward encroachment of salt marsh cordgrass in response to accelerated sea-level rise. PNAS 98, 14218–14223 (2001).ADS 
    Article 

    Google Scholar 
    Sharpe, P. J. & Baldwin, A. H. Tidal marsh plant community response to sea-level rise: A mesocosm study. Aquat. Bot. 101, 34–40 (2012).Article 

    Google Scholar 
    Birnbaum, C., Waryszak, P. & Farrer, E. C. Direct and indirect effects of climate change in coastal wetlands: Will climate change influence wetlands by affecting plant invasion?. Wetlands 59, 1–11 (2021).
    Google Scholar 
    Noto, A. E. & Shurin, J. B. Early stages of sea-level rise lead to decreased salt marsh plant diversity through stronger competition in Mediterranean climate marshes. PLoS ONE 12, 1–11 (2017).Article 

    Google Scholar 
    Stagg, C. L., Baustian, M. M., Perry, C. L., Carruthers, T. J. B. & Hall, C. T. Direct and indirect controls on organic matter decomposition in four coastal wetland communities along a landscape salinity gradient. J. Ecol. 106, 655–670 (2017).Article 

    Google Scholar 
    Neubauer, S. C., Piehler, M. F., Smyth, A. R. & Franklin, R. B. Saltwater intrusion modifies microbial community structure and decreases denitrification in tidal freshwater marshes. Ecosystems 22, 912–928 (2019).CAS 
    Article 

    Google Scholar 
    Rath, K. M., Fierer, N., Murphy, D. V. & Rousk, J. Linking bacterial community composition to soil salinity along environmental gradients. ISME. 13, 836–846 (2019).CAS 
    Article 

    Google Scholar 
    Meyerson, L. A., Cronin, J. T. & Pysek, P. Phragmites australis as a model organism for studying plant invasions. Biol. Invasions 18, 2421–2431 (2016).Article 

    Google Scholar 
    Soares, M. A. et al. Evaluation of the functional roles of fungal endophytes of Phragmites australis from high saline and low saline habitats. Biol. Invasions 18, 2689–2702 (2016).Article 

    Google Scholar 
    Gonzalez, M., Baldwin, A. H., Maul, J. E. & Yarwood, S. A. Dark septate endophyte improves salt tolerance of native and invasive lineages of Phragmites australis. ISME 14, 1943–1954 (2020).Article 

    Google Scholar 
    Farrer, E. C. et al. Plant and microbial impacts of an invasive species vary across an environmental gradient. J. Ecol. 109, 2163–2176 (2021).Article 

    Google Scholar 
    Callaway, R. M., Thelen, G. C., Rodriguez, A. & Holben, W. E. Soil biota and exotic plant invasion. Nature 427, 731–733 (2004).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Smith, L. M. & Reynolds, H. L. Plant–soil feedbacks shift from negative to positive with decreasing light in forest understory species. Ecology 96, 2523–2532 (2015).PubMed 
    Article 

    Google Scholar 
    Parepa, M., Schaffner, U. & Bossdorf, O. Help from underground: Soil biota facilitate knotweed invasion. Ecosphere 4, 1–11 (2013).Article 

    Google Scholar 
    Larios, L. & Suding, K. N. Competition and soil resource environment alter plant-soil feedbacks for native and exotic grasses. AoB Plants 7, 1–9 (2014).
    Google Scholar 
    Hoeksema, J. D. Ongoing coevolution in mycorrhizal interactions. New Phytol. 187, 286–300 (2010).PubMed 
    Article 

    Google Scholar 
    Van der Heijden, M. G. A., Martin, F. M., Selosse, M. & Sanders, I. R. Mycorrhizal ecology and evolution: The past, the present, and the future. New Phytol. 205, 1406–1423 (2015).PubMed 
    Article 

    Google Scholar 
    Hoeksema, J. D. et al. Evolutionary history of plant hosts and fungal symbionts predicts the strength of mycorrhizal mutualism. Commun. Biol. 1(116), 2018. https://doi.org/10.1038/s42003-018-0120-9 (2018).Article 

    Google Scholar 
    Remke, M. J., Johnson, N. C., Wright, J., Williamson, M. & Bowker, M. A. Sympatric pairings of dryland grass populations, mycorrhizal fungi and associated soil biota enhance mutualism and ameliorate drought stress. J. Ecol. 109, 1210–1223 (2020).Article 

    Google Scholar 
    Farrer, E. C. & Suding, K. N. Teasing apart plant community responses to N enrichment: The roles of resource limitation, competition and soil microbes. Ecol. Lett. 19, 1287–1296 (2016).PubMed 
    Article 

    Google Scholar 
    Hawkins, A. P. & Crawford, K. M. Interactions between plants and soil microbes may alter the relative importance of intraspecific and interspecific plant competition in a changing climate. AoB Plants. 10, 39. https://doi.org/10.1093/aobpla/ply039 (2018).Article 

    Google Scholar 
    Wu, Y. et al. Long-term nitrogen and sulfur deposition increased root-associated pathogen diversity and changed mutualistic fungal diversity in a boreal forest. Soil Biol. Biogeochem. 115, 108163. https://doi.org/10.1016/j.soilbio.2021.108163 (2021).CAS 
    Article 

    Google Scholar 
    Allen, W. J., Meyerson, L. A., Flick, A. J. & Cronin, J. T. Intraspecific variation in indirect plant–soil feedbacks influences a wetland plant invasion. Ecology 99, 1430–1440 (2018).PubMed 
    Article 

    Google Scholar 
    Crawford, K. M. & Knight, T. M. Competition overwhelms the positive plant-soil feedback generated by an invasive plant. Oecologia 183, 211–220 (2017).ADS 
    PubMed 
    Article 

    Google Scholar 
    Bertness, M. D. & Shumway, S. W. Competition and facilitation in marsh plants. Am. Nat. 142, 718–724 (1993).CAS 
    PubMed 
    Article 

    Google Scholar 
    Uddin, M. N., Robinson, R. W., Buultjens, A., Al-Harun, M. A. Y. & Shampa, S. H. Role of allelopathy of Phragmites australis in its invasion processes. J. Exp. Mar. Biol. Ecol. 486, 237–244 (2017).Article 

    Google Scholar 
    Howard, R. J. & Rafferty, P. S. Clonal variation in response to salinity and flooding stress in four marsh macrophytes of the northern gulf of Mexico, USA. Environ. Exp. Bot. 56, 301–313 (2006).Article 

    Google Scholar 
    Visser, J. M., Sasser, C. E., Chabreck, R. H. & Linscombe, R. G. Marsh vegetation types of the Mississippi River Deltaic plain. Estuaries 21, 818–828 (1998).Article 

    Google Scholar 
    De Wit, C. T. & van den Bergh, J. P. Competition between herbage plants. NJAS 13, 212–221 (1965).Article 

    Google Scholar 
    R Core Team. In r: A Language and Environment for Statistical Computing; r foundation for statistical computing: Vienna, Austria (2017).Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2016).MATH 
    Book 

    Google Scholar  More

  • in

    This rare primate will not survive deforestation

    .readcube-buybox { display: none !important;}
    An endangered lemur species that lives in Madagascar’s rainforest could vanish within 25 years if deforestation on the island isn’t reduced1.

    Access options

    /* style specs start */
    style{display:none!important}.LiveAreaSection-193358632 *{align-content:stretch;align-items:stretch;align-self:auto;animation-delay:0s;animation-direction:normal;animation-duration:0s;animation-fill-mode:none;animation-iteration-count:1;animation-name:none;animation-play-state:running;animation-timing-function:ease;azimuth:center;backface-visibility:visible;background-attachment:scroll;background-blend-mode:normal;background-clip:borderBox;background-color:transparent;background-image:none;background-origin:paddingBox;background-position:0 0;background-repeat:repeat;background-size:auto auto;block-size:auto;border-block-end-color:currentcolor;border-block-end-style:none;border-block-end-width:medium;border-block-start-color:currentcolor;border-block-start-style:none;border-block-start-width:medium;border-bottom-color:currentcolor;border-bottom-left-radius:0;border-bottom-right-radius:0;border-bottom-style:none;border-bottom-width:medium;border-collapse:separate;border-image-outset:0s;border-image-repeat:stretch;border-image-slice:100%;border-image-source:none;border-image-width:1;border-inline-end-color:currentcolor;border-inline-end-style:none;border-inline-end-width:medium;border-inline-start-color:currentcolor;border-inline-start-style:none;border-inline-start-width:medium;border-left-color:currentcolor;border-left-style:none;border-left-width:medium;border-right-color:currentcolor;border-right-style:none;border-right-width:medium;border-spacing:0;border-top-color:currentcolor;border-top-left-radius:0;border-top-right-radius:0;border-top-style:none;border-top-width:medium;bottom:auto;box-decoration-break:slice;box-shadow:none;box-sizing:border-box;break-after:auto;break-before:auto;break-inside:auto;caption-side:top;caret-color:auto;clear:none;clip:auto;clip-path:none;color:initial;column-count:auto;column-fill:balance;column-gap:normal;column-rule-color:currentcolor;column-rule-style:none;column-rule-width:medium;column-span:none;column-width:auto;content:normal;counter-increment:none;counter-reset:none;cursor:auto;display:inline;empty-cells:show;filter:none;flex-basis:auto;flex-direction:row;flex-grow:0;flex-shrink:1;flex-wrap:nowrap;float:none;font-family:initial;font-feature-settings:normal;font-kerning:auto;font-language-override:normal;font-size:medium;font-size-adjust:none;font-stretch:normal;font-style:normal;font-synthesis:weight style;font-variant:normal;font-variant-alternates:normal;font-variant-caps:normal;font-variant-east-asian:normal;font-variant-ligatures:normal;font-variant-numeric:normal;font-variant-position:normal;font-weight:400;grid-auto-columns:auto;grid-auto-flow:row;grid-auto-rows:auto;grid-column-end:auto;grid-column-gap:0;grid-column-start:auto;grid-row-end:auto;grid-row-gap:0;grid-row-start:auto;grid-template-areas:none;grid-template-columns:none;grid-template-rows:none;height:auto;hyphens:manual;image-orientation:0deg;image-rendering:auto;image-resolution:1dppx;ime-mode:auto;inline-size:auto;isolation:auto;justify-content:flexStart;left:auto;letter-spacing:normal;line-break:auto;line-height:normal;list-style-image:none;list-style-position:outside;list-style-type:disc;margin-block-end:0;margin-block-start:0;margin-bottom:0;margin-inline-end:0;margin-inline-start:0;margin-left:0;margin-right:0;margin-top:0;mask-clip:borderBox;mask-composite:add;mask-image:none;mask-mode:matchSource;mask-origin:borderBox;mask-position:0 0;mask-repeat:repeat;mask-size:auto;mask-type:luminance;max-height:none;max-width:none;min-block-size:0;min-height:0;min-inline-size:0;min-width:0;mix-blend-mode:normal;object-fit:fill;object-position:50% 50%;offset-block-end:auto;offset-block-start:auto;offset-inline-end:auto;offset-inline-start:auto;opacity:1;order:0;orphans:2;outline-color:initial;outline-offset:0;outline-style:none;outline-width:medium;overflow:visible;overflow-wrap:normal;overflow-x:visible;overflow-y:visible;padding-block-end:0;padding-block-start:0;padding-bottom:0;padding-inline-end:0;padding-inline-start:0;padding-left:0;padding-right:0;padding-top:0;page-break-after:auto;page-break-before:auto;page-break-inside:auto;perspective:none;perspective-origin:50% 50%;pointer-events:auto;position:static;quotes:initial;resize:none;right:auto;ruby-align:spaceAround;ruby-merge:separate;ruby-position:over;scroll-behavior:auto;scroll-snap-coordinate:none;scroll-snap-destination:0 0;scroll-snap-points-x:none;scroll-snap-points-y:none;scroll-snap-type:none;shape-image-threshold:0;shape-margin:0;shape-outside:none;tab-size:8;table-layout:auto;text-align:initial;text-align-last:auto;text-combine-upright:none;text-decoration-color:currentcolor;text-decoration-line:none;text-decoration-style:solid;text-emphasis-color:currentcolor;text-emphasis-position:over right;text-emphasis-style:none;text-indent:0;text-justify:auto;text-orientation:mixed;text-overflow:clip;text-rendering:auto;text-shadow:none;text-transform:none;text-underline-position:auto;top:auto;touch-action:auto;transform:none;transform-box:borderBox;transform-origin:50% 50%0;transform-style:flat;transition-delay:0s;transition-duration:0s;transition-property:all;transition-timing-function:ease;vertical-align:baseline;visibility:visible;white-space:normal;widows:2;width:auto;will-change:auto;word-break:normal;word-spacing:normal;word-wrap:normal;writing-mode:horizontalTb;z-index:auto;-webkit-appearance:none;-moz-appearance:none;-ms-appearance:none;appearance:none;margin:0}.LiveAreaSection-193358632{width:100%}.LiveAreaSection-193358632 .login-option-buybox{display:block;width:100%;font-size:17px;line-height:30px;color:#222;padding-top:30px;font-family:Harding,Palatino,serif}.LiveAreaSection-193358632 .additional-access-options{display:block;font-weight:700;font-size:17px;line-height:30px;color:#222;font-family:Harding,Palatino,serif}.LiveAreaSection-193358632 .additional-login >li:not(:first-child)::before{transform:translateY(-50%);content:””;height:1rem;position:absolute;top:50%;left:0;border-left:2px solid #999}.LiveAreaSection-193358632 .additional-login >li:not(:first-child){padding-left:10px}.LiveAreaSection-193358632 .additional-login >li{display:inline-block;position:relative;vertical-align:middle;padding-right:10px}.BuyBoxSection-683559780{display:flex;flex-wrap:wrap;flex:1;flex-direction:row-reverse;margin:-30px -15px 0}.BuyBoxSection-683559780 .box-inner{width:100%;height:100%}.BuyBoxSection-683559780 .readcube-buybox{background-color:#f3f3f3;flex-shrink:1;flex-grow:1;flex-basis:255px;background-clip:content-box;padding:0 15px;margin-top:30px}.BuyBoxSection-683559780 .subscribe-buybox{background-color:#f3f3f3;flex-shrink:1;flex-grow:4;flex-basis:300px;background-clip:content-box;padding:0 15px;margin-top:30px}.BuyBoxSection-683559780 .subscribe-buybox-nature-plus{background-color:#f3f3f3;flex-shrink:1;flex-grow:4;flex-basis:100%;background-clip:content-box;padding:0 15px;margin-top:30px}.BuyBoxSection-683559780 .title-readcube{display:block;margin:0;margin-right:20%;margin-left:20%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .title-buybox{display:block;margin:0;margin-right:29%;margin-left:29%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .title-asia-buybox{display:block;margin:0;margin-right:5%;margin-left:5%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .asia-link{color:#069;cursor:pointer;text-decoration:none;font-size:1.05em;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:1.05em6}.BuyBoxSection-683559780 .access-readcube{display:block;margin:0;margin-right:10%;margin-left:10%;font-size:14px;color:#222;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .access-asia-buybox{display:block;margin:0;margin-right:5%;margin-left:5%;font-size:14px;color:#222;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .access-buybox{display:block;margin:0;margin-right:30%;margin-left:30%;font-size:14px;color:#222;opacity:.8px;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .usps-buybox{display:block;margin:0;margin-right:30%;margin-left:30%;font-size:14px;color:#222;opacity:.8px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .price-buybox{display:block;font-size:30px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;padding-top:30px;text-align:center}.BuyBoxSection-683559780 .price-from{font-size:14px;padding-right:10px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .issue-buybox{display:block;font-size:13px;text-align:center;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:19px}.BuyBoxSection-683559780 .no-price-buybox{display:block;font-size:13px;line-height:18px;text-align:center;padding-right:10%;padding-left:10%;padding-bottom:20px;padding-top:30px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif}.BuyBoxSection-683559780 .vat-buybox{display:block;margin-top:5px;margin-right:20%;margin-left:20%;font-size:11px;color:#222;padding-top:10px;padding-bottom:15px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:17px}.BuyBoxSection-683559780 .button-container{display:flex;padding-right:20px;padding-left:20px;justify-content:center}.BuyBoxSection-683559780 .button-container >*{flex:1px}.BuyBoxSection-683559780 .button-container >a:hover,.Button-505204839:hover,.Button-1078489254:hover,.Button-2808614501:hover{text-decoration:none}.BuyBoxSection-683559780 .readcube-button{background:#fff;margin-top:30px}.BuyBoxSection-683559780 .button-asia{background:#069;border:1px solid #069;border-radius:0;cursor:pointer;display:block;padding:9px;outline:0;text-align:center;text-decoration:none;min-width:80px;margin-top:75px}.BuyBoxSection-683559780 .button-label-asia,.ButtonLabel-3869432492,.ButtonLabel-3296148077,.ButtonLabel-1566022830{display:block;color:#fff;font-size:17px;line-height:20px;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;text-align:center;text-decoration:none;cursor:pointer}.Button-505204839,.Button-1078489254,.Button-2808614501{background:#069;border:1px solid #069;border-radius:0;cursor:pointer;display:block;padding:9px;outline:0;text-align:center;text-decoration:none;min-width:80px;max-width:320px;margin-top:10px}.Button-505204839 .readcube-label,.Button-1078489254 .readcube-label,.Button-2808614501 .readcube-label{color:#069}
    /* style specs end */Subscribe to Nature+Get immediate online access to the entire Nature family of 50+ journals$29.99monthlySubscribe to JournalGet full journal access for 1 year$199.00only $3.90 per issueAll prices are NET prices.VAT will be added later in the checkout.Tax calculation will be finalised during checkout.Buy articleGet time limited or full article access on ReadCube.$32.00All prices are NET prices.

    Additional access options:

    doi: https://doi.org/10.1038/d41586-022-03116-6

    References

    Subjects

    Conservation biology More

  • in

    Predicting performance of naïve migratory animals, from many wrongs to self-correction

    Calculation of flight-step headings and movementTerms defining flight-step movement, precision and geophysical orientation cues are listed in Table 1. Since seasonal migration nearly ubiquitously proceeds from higher to lower latitudes, it is convenient to define headings clockwise from geographic South (counter-clockwise from geographic North for migration commencing in the Southern Hemisphere). Assuming a spherical Earth, a sequence of N migratory flight-steps with corresponding headings, αi, i = 0,…, N−1, the latitudes, ∅i+1, and longitudes, λi+1, on completion of each flight-step can be calculated using the Haversine Equation76, which we approximated by stepwise planar movement using Eqs. (1) and (2). For improved computational accuracy and to accommodate within flight-step effects, we updated simulated headings and corresponding locations hourly. A migrant’s flight-step distance ({R}_{{{mathrm {step}}}}=3.6{V}_{{mathrm {a}}}{cdot n}_{{mathrm {H}}}/{R}_{{{mathrm {Earth}}}}) (in radians), depends on its flight speed, Va (m/s) relative to the mean Earth radius REarth (km), and flight-step hours, nH. With a geomagnetic in-flight compass, expected hourly geographic headings are modulated by changes in magnetic declination, i.e., the clockwise difference between geographic and geomagnetic South10,32.Formulation of compass coursesFor simplicity, we consider the case of a single inherited or imprinted heading. This can be extended to include sequences of preferred headings. Expected geographic loxodrome headings remain unchanged en route, i.e.,$${bar{{{{{{rm{alpha }}}}}}}}_{i}={bar{{{{{{rm{alpha }}}}}}}}_{0}$$
    (5)
    Relative to geographic axes, expected geomagnetic loxodrome headings remain unchanged relative to proximate geomagnetic South, i.e., are offset by geomagnetic declination on departure (updated hourly in simulations)$${bar{{{{{{rm{alpha }}}}}}}}_{i}={bar{{{{{{rm{alpha }}}}}}}}_{0}+{delta }_{{mathrm {m}},i}$$
    (6)
    As described and illustrated in detail by Kiepenheuer13, the magnetoclinic compass was hypothesized to explain the prevalence of “curved” migratory bird routes, i.e., for which local geographic headings shift gradually but substantially en route. A migrant with a magnetoclinic compass adjusts its heading at each flight-step to maintain a constant transverse component, γ′, of the experienced inclination angle, γ, so that error-free headings are (see Fig. S5 in ref. 34)$${{bar{{{{{{rm{alpha }}}}}}}}_{i}={{sin }}}^{-1}left(frac{{{tan }}{gamma }_{i}}{{{tan }}{gamma }^{{prime} }}right){={{sin }}}^{-1}left(frac{{{tan }}{gamma }_{i}{{sin }}{bar{{{{{{rm{alpha }}}}}}}}_{0}}{{{tan }}{gamma }_{0}}right).$$
    (7)
    In a geomagnetic dipole field, the horizontal (Bh) and vertical (Bz) field, and therefore also inclination, each depends solely on geomagnetic latitude, ∅m:(gamma ={{{tan }}}^{-1}left({B}_{{mathrm {z}}}/{B}_{{mathrm {h}}}right)={{{tan }}}^{-1}left(2{{sin }}{phi }_{{mathrm {m}}}/{{cos }}{phi }_{{mathrm {m}}}right)={{{tan }}}^{-1}left(2{{tan }}{phi }_{{mathrm {m}}}right).) The projected transverse component, therefore, becomes$${gamma }^{{prime} }={{{tan }}}^{-1}left(frac{{{tan }}{gamma }_{0}}{{{sin }}{bar{{{alpha }}}}_{0}}right)={{{tan }}}^{-1}left(frac{2{{tan }}{{{phi }}}_{{mathrm {m}},0}}{{{sin }}{bar{{{{{{rm{alpha }}}}}}}}_{0}}right),$$which can be substituted into Eq. (7) to produce a closed formula for magnetoclinic headings in a dipole as a function of geomagnetic latitude$${bar{{{{{{rm{alpha }}}}}}}}_{i}left({{{phi }}}_{{mathrm {m}},i}right)={{{sin }}}^{-1}left(frac{{{sin }}{bar{{{{{{rm{alpha }}}}}}}}_{0}}{{{tan }}{{{phi }}}_{{mathrm {m}},0}}cdot {{tan }}{{{phi }}}_{{mathrm {m}},i}right),$$
    (8)
    with the expected initial heading, ({bar{{{{{{rm{alpha }}}}}}}}_{0}), and initial geomagnetic latitude, ∅m,0, being constants. Equations (7) and (8) have no solution when inclination increases en route, which could occur following substantial orientation error or in strongly non-dipolar fields. We followed previous studies in allowing magnetoclinic migrants to head towards magnetic East or West until inclination decreased sufficiently33,34,46, but also included orientation error based on the modelled compass precision.To assess sun-compass sensitivity algebraically, and also to improve computational efficiency, we used a closed-form equation for sunset azimuth, θs (derived in Supplementary Note 3 and see ref. 23),$${theta }_{{mathrm {s}}}={{{cos }}}^{-1}left(frac{-{{sin }}{delta }_{{mathrm {s}}}}{{{cos }}{{phi }}}right),$$
    (9)
    where δs is the solar declination, which varies between −23.4° and 23.4° with season and latitude23. Sunset azimuth is the positive and sunrise azimuth is the negative solution to Eq. (9) (relative to geographic N–S).Fixed sun-compass headings represent a uniform (clockwise) offset, ({bar{{{{{{rm{alpha }}}}}}}}_{{mathrm {s}}}) to sunrise or sunset azimuth, θs,i (calculated using Eq. (9))$${{bar{{{{{{rm{alpha }}}}}}}}_{i}={bar{{{{{{rm{alpha }}}}}}}}_{{mathrm {s}}}+theta }_{{mathrm {s}},i}$$
    (10)
    where the preferred heading on commencement of migration, ({bar{{{{{{rm{alpha }}}}}}}}_{{mathrm {s}}}={bar{{{{{{rm{alpha }}}}}}}}_{0}-{theta }_{{mathrm {s}},0}), is presumed to be imprinted using an inherited geographic or geomagnetic heading2,10,30.With a TCSC, preferred headings relative to sun azimuth are adjusted according to the time of day. In the context of sun-compass use during migration, Alerstam and Pettersson22 related the hourly “clock-shift” induced by crossing bands of longitude (∆h = 12 ∆λ/π), to a migrant’s time-compensated adjustment given the rate of change (i.e., angular speed) of sun azimuth close to sunset$$frac{partial {theta }_{{mathrm {s}}}}{partial h}cong frac{2pi {{sin }}{{phi }}}{24},$$
    (11)
    resulting in a “time-compensated” offset in heading on departure ((varDelta bar{{{{{{rm{alpha }}}}}}}cong varDelta {{{{{rm{lambda }}}}}},sin phi), which Eq.(4)). Equation (4) results in near-great-circle trajectories for small ranges in latitude, ∅, until inner clocks are reset. The feasibility of TCSC courses over longer distances (latitude ranges) relies on two critical but little-explored assumptions: (1) time-compensated orientation adjustments are presumed to follow the angular speed of sun azimuth (Eq. (11)) retained from the most recent clock-reset site, and (2) to negotiate unpredictable migratory schedules, migrants are presumed to retain their preferred geographic heading on arrival at extended stopovers22.Regarding the first assumption, time-compensated adjustments could also be influenced by proximate speeds of sun azimuth even when inner clocks are not fully reset. We, therefore, use distinct indices to keep track of “reference” flight-steps for clock-resets (cref,i) and time-compensated adjustments (sref,i). TCSC flight-step headings can then be written as$${bar{{{{{{rm{alpha }}}}}}}}_{i}=left{begin{array}{cc}{bar{{{{{{rm{alpha }}}}}}}}_{{c}_{{{mathrm {ref}}},i}}+left({theta }_{{mathrm {s}},i}-{theta }_{{mathrm {s}},{c}_{{{mathrm {ref}}},i}}right)+left({{{{{{rm{lambda }}}}}}}_{i}-{{{{{{rm{lambda }}}}}}}_{{c}_{{{mathrm {ref}}},i}}right){{sin }}{phi }_{{s}_{{{mathrm {ref}}},i}}, & {i,ne, c}_{{{mathrm {ref}}},i} ; (12a)\ {{{{{{rm{alpha }}}}}}}_{i-1}, & {i=c}_{{{mathrm {ref}}},i} ; (12b)end{array}right.,$$where θs,i represents the sunset azimuth on departures, cref,i specifies the most recent clock-reset site (during which geographic headings are also retained, i.e., ({bar{{{{{{rm{alpha }}}}}}}}_{i}={{{{{{rm{alpha }}}}}}}_{i-1})), and sref,i specifies the site defining the migrant’s temporal (hourly) rate of “time-compensated” adjustments (Eq. (11)). For TCSC courses as conceived by Alerstam and Pettersson22, reference rates of adjustment to sun azimuth are reset in tandem during stopovers, i.e., ({s}_{{{mathrm {ref}}},i}={c}_{{{mathrm {ref}}},i}), but we also considered a proximately gauged TCSC, where migrants gauge their adjustments to currently experienced speed of sun azimuth, i.e., ({s}_{{{mathrm {ref}}},i}=i).Regarding the second assumption, retaining geographic headings on arrival at stopovers is not consistent with ignoring geographic headings between consecutive nightly flight-steps, and may be difficult to achieve while landing. We, therefore, examined a more parsimonious alternative (Fig. 7d, Supplementary Fig. 3) where migrants retain their (usual) TCSC heading from the first night of stopovers, i.e., as if they would have departed on the first night. This alternative also simplifies Eq. (12) to$${bar{{{{{{rm{alpha }}}}}}}}_{i}={bar{{{{{{rm{alpha }}}}}}}}_{{c}_{{{mathrm {ref}}},i}}+left({theta }_{{mathrm {s}},({t}_{i-1}+1)}-{theta }_{{mathrm {s}},{t}_{i-1}}right)+left({{{{{{rm{lambda }}}}}}}_{i}-{{{{{{rm{lambda }}}}}}}_{{c}_{{{mathrm {ref}}},i}}right){{sin }}{{{phi }}}_{{s}_{{{mathrm {ref}}},i}}$$
    (12c)
    where the index ti−1 here represents the departure date from the previous flight.Sensitivity of compass-course headingsSensitivity was assessed by the marginal change in expected heading from previous (imprecise) headings, (partial {bar{alpha }}_{i}/partial {alpha }_{i-1}). When this is positive, small errors in headings will perpetuate, and therefore expected errors in migratory trajectories will grow iteratively. Conversely, negative sensitivity implies self-correction between successive flight-steps. Geographic and geomagnetic loxodromes are per definition constant relative to their respective axes so have “zero” sensitivity, as long as cue-detection errors are stochastically independent.For magnetoclinic compass courses in a dipole field, sensitivity can be calculated by differentiating Eq. (8) with respect to previous headings:$$frac{{mathrm {d}}{bar{{{{{{rm{alpha }}}}}}}}_{i}}{{mathrm {d}}{{{{{{rm{alpha }}}}}}}_{i-1}}=frac{{sin bar{{{{{{rm{alpha }}}}}}}}_{0}}{tan {phi }_{{mathrm {m}},0}}cdot frac{1}{cos {bar{alpha }}_{i}{cos }^{2}{phi }_{{mathrm {m}},i}}frac{partial {phi }_{{mathrm {m}},i}}{partial {alpha }_{i-1}}=frac{{R}_{{mathrm {step}}},sin {alpha }_{i-1}{sin bar{{{{{{rm{alpha }}}}}}}}_{0}}{cos {bar{alpha }}_{i}{cos }^{2}{phi }_{{mathrm {m}},i},tan {phi }_{{mathrm {m}},0}}$$
    (13)
    All three terms in the denominator indicate, as illustrated in Fig. 3b, that magnetoclinic courses become unstably sensitive at both high and low latitudes, and any heading with a significantly East–West component.Sensitivity of fixed sun compass headings is non-zero due to sun azimuth dependence on location (Eq. (9)):$$frac{{mathrm {d}}{bar{{{{{{rm{alpha }}}}}}}}_{i}}{{mathrm {d}}{{{{{{rm{alpha }}}}}}}_{i-1}} = , frac{sin {delta }_{{mathrm {s}},i}}{sin {theta }_{{mathrm {s}},i}}cdot frac{sin {phi }_{i}}{{cos }^{2}{phi }_{i}}frac{partial {phi }_{i}}{partial {alpha }_{i-1}}=frac{sin {delta }_{{mathrm {s}},i}}{sin {theta }_{{mathrm {s}},i}}cdot frac{{R}_{{mathrm {step}}},sin {phi }_{i},sin {alpha }_{i-1}}{{cos }^{2}{phi }_{i}}\ = , {R}_{{mathrm {step}}}cdot ,sin {alpha }_{i-1}frac{tan {phi }_{i}}{tan {theta }_{{mathrm {s}},i}}$$
    (14)
    The sine factor on the right-hand side in Eq. (14) causes the sign of (partial {bar{alpha }}_{i}/partial {alpha }_{i-1}) to be opposite for East to West or West to East headings, and tan θs also change sign at the fall equinox (due to solar declination changing sign). The azimuth term in the denominator indicates heightened sensitivity closer to the summer or winter equinox and at high latitudes, and, conversely, heightened robustness to errors closer to the spring or autumnal equinox (since ({{tan }}{theta }_{{mathrm {s}},0}to pm infty)). This seasonal and directional asymmetry is illustrated in Fig. 3c, e.TCSC courses (Eq. (12)) involve up to three sensitivity terms, due to dependencies on sun azimuth, longitude and latitude:$$ frac{{mathrm {d}}{bar{{{{{{rm{alpha }}}}}}}}_{i}}{{mathrm {d}}{{{{{{rm{alpha }}}}}}}_{i-1}} = , {R}_{{{mathrm {step}}}}cdot {{sin }}{alpha }_{i-1}frac{{{tan }}{phi }_{i}}{{{tan }}{theta }_{{mathrm {s}},i}}+frac{{mathrm {d}}{lambda }_{i}}{{mathrm {d}}{{{{{{rm{alpha }}}}}}}_{i-1}}{{sin }}{{{phi }}}_{{c}_{{{mathrm {ref}}}},i}+left({{{{{{rm{lambda }}}}}}}_{i}-{{{{{{rm{lambda }}}}}}}_{{c}_{{{mathrm {ref}}}},i}right)frac{{mathrm {d}}{{sin }}{phi }_{{s}_{{{mathrm {ref}}}},i}}{{mathrm {d}}{{{{{{rm{alpha }}}}}}}_{i-1}}\ =, left{begin{array}{cc}{R}_{{{mathrm {step}}}}cdot left[{{sin }}{alpha }_{i-1}frac{{{tan }}{phi }_{i}}{{{tan }}{theta }_{{mathrm {s}},i}}-frac{{{cos }}{{{{{{rm{alpha }}}}}}}_{i-1}{{sin }}{phi }_{{s}_{{{mathrm {ref}}}},i}}{{{cos }}{phi }_{i-1}}right],hfill & {{{{{rm{classic}}}}}} ; (15{{{{{rm{a}}}}}})\ {R}_{{{mathrm {step}}}}left[{{sin }}{alpha }_{i-1}frac{{{tan }}{phi }_{i}}{{{tan }}{theta }_{{mathrm {s}},i}}-frac{{{cos }}{{{{{{rm{alpha }}}}}}}_{i-1}{{sin }}{phi }_{{s}_{{{mathrm {ref}}}},i}}{{{cos }}{phi }_{i-1}}+left({{{{{{rm{lambda }}}}}}}_{i}-{{{{{{rm{lambda }}}}}}}_{{c}_{{{mathrm {ref}}}},i}right){{sin }}{alpha }_{i-1}{{cos }}{phi }_{i}right], & {{{{{rm{proximate}}}}}} ; left(15{{{{{rm{b}}}}}}right).end{array}right.$$The first square-bracketed terms in Eqs. (15a, b) are identical to the fixed sun compass (Eq. (14)), reflecting seasonal and latitudinal dependence in sun-azimuth. For headings with a Southward component (α0  1) and nonexistent for North–South headings (G = 1, reflecting no longitude bands being crossed). We expected this factor to affect compass courses differentially according to their error-accumulating or self-correcting nature.We further modified the effective goal-area breadth to account for a (geographically) circular goal area on the sphere, i.e., effectively modulating the longitudinal component of the goal-area breadth at the arrival latitude, ∅A:$${beta }_{{mathrm {A}}}=beta sqrt{{{{{sin }}}^{2}bar{alpha }+left({{cos }}bar{alpha }/{{cos }}{{{phi }}}_{{mathrm {A}}}right)}^{2}}.$$
    (19)
    To account for differential sensitivity among compass-courses, we generalized the normal many-wrongs relation between performance and number of steps, (1/{hat{N}}^{eta }), from η = 0.5 (Eqs. (3) and (16)) to$$eta left({sigma }_{{step}}|s,bright)=left(0.5+bright){e}^{-s{{sigma }_{{step}}}^{2}},$$
    (20)
    where b  0 self-correction, and s represents a modulating exponential damping factor, consistent with the limiting circular-uniform case (as κ → 0, i.e., ({sigma }_{{{mathrm {step}}}}to infty)), where no (timely) convergence of heading is expected with an increasing number of steps.In assessing performance, we also accounted for seasonal migration constraints via a population-specific maximum number of steps, Nmax (Table 2; this became significant for the longest-distance simulations with large expected errors, i.e., small ({{{{{{rm{kappa }}}}}}}_{{{mathrm {step}}}}=1/{sigma }_{{{mathrm {step}}}}^{2})). The probability of having arrived at the goal latitude can be estimated using the Central Limit Theorem:$${p}_{{{phi }},{N}_{{max }}}cong frac{1}{2}left[1-{erf}left(left(frac{{N}_{0}}{{N}_{{max }}}-frac{{I}_{1}left({{{{{{rm{kappa }}}}}}}_{{{mathrm {step}}}}right)}{{I}_{0}left({{{{{{rm{kappa }}}}}}}_{{{mathrm {step}}}}right)}right)cdot frac{{{cos }}bar{alpha }}{{sigma }_{{mathrm {C}}}sqrt{2}}right)right],$$
    (21)
    where Ij is the modified Bessel function of the first kind and order j53, and σC (the standard deviation in the latitudinal component of flight-step distance) can be calculated using Bessel functions together with known properties of sums of cosines53,77 (Supplementary Note 2).Regression-estimated performanceWe fit the parameters in the spherical-geometry factor (Eq. (18)) and many-wrongs effect (Eq. (20)) according to expected performance, estimated as the product of sufficiently timely migration (Eq. (21)) and sufficiently precise migration, now generalized from Eq. (16), i.e.$${p}_{beta ,hat{N}}cong {erf}left(frac{{beta }_{{mathrm {A}}}}{{G}^{{g}}sqrt{2left({{sigma }_{{{mathrm {ind}}}}}^{2}+{sigma }_{{{mathrm {step}}}}/{hat{N}}^{n}right)}}right),$$
    (22)
    This resulted in up to four fitted parameters for each compass course

    i.

    an exponent, g, to the spherical-geometry factor (Eq. (19)), i.e., Gg, reflecting how growth or self-correction in errors between steps further augments or reduces this factor,

    ii.

    a baseline offset, b0, to the “normal” exponent η = 0.5, which mediates the relation between the number of steps and performance (Eq. (20)),

    iii.

    an exponent s reflecting how decreasing precision among flight-steps dampens the many-wrongs convergence (Eq. (20)),

    iv.

    for TCSC courses, a modulation, ρ, to the offset, b0, quantifying the extent to which self-correction increases with increased flight-step distance Rstep, i.e., ({{b={b}_{0}R}_{{{mathrm {step}}}}^{{prime} }}^{rho }) in Eq. (20), where ({R}_{{{mathrm {step}}}}^{{prime} })is the flight-step distance scaled by its median value among species.

    Parameters were fit using MATLAB routine fitnlm based on compass course performance among species and seven error scenarios (5°, 10°, 20°, 30°, 40°, 50°, and 60° directional precision among flight-steps), for all combinations (including or excluding the four parameters). The most parsimonious combination of parameters was selected using MATLAB routine aicbic, based on the AICc, the Akaike information criterion corrected for small sample size57. Null values for the spherical-geometry parameter were set to g = 1, and for the parameters governing convergence of route-mean headings b0 = 0, s = 0, and, for TCSC courses, ρ = 0 (for loxodrome courses, ρ = 0 by default, i.e., was not fitted).Statistics and reproducibilityOur simulation results, regression fitting and AICc-model selection are reproducible using the MATLAB scripts (see the section “Code availability”).Reporting summaryFurther information on research design is available in the Nature Research Reporting Summary linked to this article. More

  • in

    A tripartite model system for Southern Ocean diatom-bacterial interactions reveals the coexistence of competing symbiotic strategies

    Saba GK, Fraser WR, Saba VS, Iannuzzi RA, Coleman KE, Doney SC, et al. Winter and spring controls on the summer food web of the coastal West Antarctic Peninsula. Nat Commun. 2014;5:4318.CAS 
    PubMed 
    Article 

    Google Scholar 
    Behrenfeld MJ, Randerson JT, McClain CR, Feldman GC, Los SO, Tucker CJ, et al. Biospheric primary production during an ENSO transition. Science. 2001;291:2594–7.CAS 
    PubMed 
    Article 

    Google Scholar 
    Amin SA, Parker MS, Armbrust EV. Interactions between diatoms and bacteria. Microbiol Mol Biol Rev. 2012;76:667–84.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Cho BC, Azam F. Major role of bacteria in biogeochemical fluxes in the ocean’s interior. Nature. 1988;332:441–3.CAS 
    Article 

    Google Scholar 
    Amin S, Hmelo L, Van Tol H, Durham B, Carlson L, Heal K, et al. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature. 2015;522:98–101.CAS 
    PubMed 
    Article 

    Google Scholar 
    Durham BP, Sharma S, Luo H, Smith CB, Amin SA, Bender SJ, et al. Cryptic carbon and sulfur cycling between surface ocean plankton. Proc Natl Acad Sci. 2015;112:453–7.CAS 
    PubMed 
    Article 

    Google Scholar 
    Mühlenbruch M, Grossart HP, Eigemann F, Voss M. Mini‐review: Phytoplankton‐derived polysaccharides in the marine environment and their interactions with heterotrophic bacteria. Environ Microbiol. 2018;20:2671–85.PubMed 
    Article 

    Google Scholar 
    Seymour JR, Amin SA, Raina J-B, Stocker R. Zooming in on the phycosphere: the ecological interface for phytoplankton–bacteria relationships. Nat Microbiol. 2017;2:1–12.Article 

    Google Scholar 
    Azam F, Fenchel T, Field JG, Gray JS, Meyer-Reil L-A, Thingstad F. The ecological role of water-column microbes in the sea. Marine ecology progress series. 1983;10:257–63.Ratnarajah L, Blain S, Boyd PW, Fourquez M, Obernosterer I, Tagliabue A. Resource colimitation drives competition between phytoplankton and bacteria in the Southern Ocean. Geophys Res Lett. 2021;48:e2020GL088369.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Oulhen N, Schulz BJ, Carrier TJ. English translation of Heinrich Anton de Bary’s 1878 speech, ‘Die Erscheinung der Symbiose’ (‘De la symbiose’). Symbiosis. 2016;69:131–9.Article 

    Google Scholar 
    Cooper MB, Smith AG. Exploring mutualistic interactions between microalgae and bacteria in the omics age. Curr Opin Plant Biol. 2015;26:147–53.PubMed 
    Article 

    Google Scholar 
    Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG. Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature. 2005;438:90–3.CAS 
    PubMed 
    Article 

    Google Scholar 
    Cole JJ. Interactions between bacteria and algae in aquatic ecosystems. Ann Rev Ecol Syst. 1982;13:291–314.Article 

    Google Scholar 
    Durham B. Deciphering metabolic currencies that support marine microbial networks. mSystems. 2021;6:e00763-21.Bell W, Mitchell R. Chemotactic and growth responses of marine bacteria to algal extracellular products. Biol Bull. 1972;143:265–77.Article 

    Google Scholar 
    Baker LJ, Kemp PF. Exploring bacteria–diatom associations using single-cell whole genome amplification. Aquat Microb Ecol. 2014;72:73–88.Article 

    Google Scholar 
    Graff JR, Rines JE, Donaghay PL. Bacterial attachment to phytoplankton in the pelagic marine environment. Mar Ecol Prog Ser. 2011;441:15–24.Article 

    Google Scholar 
    Baker LJ, Alegado RA, Kemp PF. Response of diatom-associated bacteria to host growth state, nutrient concentrations, and viral host infection in a model system. Environ Microbiol Rep. 2016;8:917–27.PubMed 
    Article 

    Google Scholar 
    Shibl AA, Isaac A, Ochsenkühn MA, Cárdenas A, Fei C, Behringer G, et al. Diatom modulation of select bacteria through use of two unique secondary metabolites. Proc Natl Acad Sci. 2020;117:27445–55.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Leinweber K, Kroth PG. Capsules of the diatom Achnanthidium minutissimum arise from fibrillar precursors and foster attachment of bacteria. PeerJ. 2015;3:e858.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Guo S, Stevens CA, Vance TDR, Olijve LLC, Graham LA, Campbell RL, et al. Structure of a 1.5-MDa adhesin that binds its Antarctic bacterium to diatoms and ice. Sci Adv. 2017;3:e1701440.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rao D, Webb JS, Kjelleberg S. Microbial colonization and competition on the Marine Alga Ulva australis. Appl Environ Microbiol. 2006;72:5547–55.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Zhou J, Chen G-F, Ying K-Z, Jin H, Song J-T, Cai Z-H, et al. Phycosphere microbial succession patterns and assembly mechanisms in a marine Dinoflagellate bloom. Appl Environ Microbiol. 2019;85:e00349–19.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Seyedsayamdost MR, Case RJ, Kolter R, Clardy J. The Jekyll-and-Hyde chemistry of Phaeobacter gallaeciensis. Nat Chem. 2011;3:331–5.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Frölicher TL, Sarmiento JL, Paynter DJ, Dunne JP, Krasting JP, Winton M. Dominance of the Southern Ocean in anthropogenic carbon and heat uptake in CMIP5 models. J Clim. 2015;28:862–86.Article 

    Google Scholar 
    Strzepek RF, Hunter KA, Frew RD, Harrison PJ, Boyd PW. Iron‐light interactions differ in Southern Ocean phytoplankton. Limnol Oceanogr. 2012;57:1182–200.CAS 
    Article 

    Google Scholar 
    Andrew SM, Strzepek RF, M Whitney S, Chow WS, Ellwood MJ. Divergent physiological and molecular responses of light‐and iron‐limited Southern Ocean phytoplankton. Limnol Oceanogr Lett. 2022;7:150–8.CAS 
    Article 

    Google Scholar 
    Bertrand EM, Saito MA, Rose JM, Riesselman CR, Lohan MC, Noble AE, et al. Vitamin B12 and iron colimitation of phytoplankton growth in the Ross Sea. Limnol Oceanogr. 2007;52:1079–93.CAS 
    Article 

    Google Scholar 
    Bertrand EM, McCrow JP, Moustafa A, Zheng H, McQuaid JB, Delmont TO, et al. Phytoplankton–bacterial interactions mediate micronutrient colimitation at the coastal Antarctic sea ice edge. Proc Natl Acad Sci. 2015;112:9938–43.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bates SSB, Hubbard KA, Lundholm N, Montresor M, Leaw CP. Pseudo-nitzschia, Nitzschia, and domoic acid: new research since 2011. Harmful Algae. 2018;79:3–43.PubMed 
    Article 

    Google Scholar 
    Almandoz GO, Ferreyra GA, Schloss IR, Dogliotti AI, Rupolo V, Paparazzo FE, et al. Distribution and ecology of Pseudo-nitzschia species (Bacillariophyceae) in surface waters of the Weddell Sea (Antarctica). Polar Biol. 2008;31:429–42.Article 

    Google Scholar 
    Jabre LJ, Allen AE, McCain JSP, McCrow JP, Tenenbaum N, Spackeen JL, et al. Molecular underpinnings and biogeochemical consequences of enhanced diatom growth in a warming Southern Ocean. Proc Natl Acad Sci. 2021;118:e2107238118.Malviya S, Scalco E, Audic S, Vincent F, Veluchamy A, Poulain J, et al. Insights into global diatom distribution and diversity in the world’s ocean. Proc Natl Acad Sci. 2016;113:E1516–25.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Moreno CM, Lin Y, Davies S, Monbureau E, Cassar N, Marchetti A. Examination of gene repertoires and physiological responses to iron and light limitation in Southern Ocean diatoms. Polar Biol. 2018;41:679–96.Article 

    Google Scholar 
    Ellis KA, Cohen NR, Moreno C, Marchetti A. Cobalamin-independent methionine synthase distribution and influence on vitamin B12 growth requirements in marine diatoms. Protist. 2017;168:32–47.CAS 
    PubMed 
    Article 

    Google Scholar 
    Price NM, Harrison GI, Hering JG, Hudson RJ, Nirel PM, Palenik B, et al. Preparation and chemistry of the artificial algal culture medium Aquil. Biol Oceanogr. 1989;6:443–61.Article 

    Google Scholar 
    Hubbard KA, Rocap G, Armbrust EV. Inter- and intraspecific community structure within the diatom genus Pseudo-nitzschia (Bacillariophyceae). J Phycol. 2008;44:637–49.CAS 
    Article 

    Google Scholar 
    Madeira F, Park YM, Lee J, Buso N, Gur T, Madhusoodanan N, et al. The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res. 2019;47:W636–41.CAS 
    PubMed 
    PubMed Central 
    Article 

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

    Google Scholar 
    Brand LE, Guillard RR, Murphy LS. A method for the rapid and precise determination of acclimated phytoplankton reproduction rates. J Plankton Res. 1981;3:193–201.Article 

    Google Scholar 
    Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ. Jalview Version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics. 2009;25:1189–91.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Nguyen L-T, Schmidt HA, Von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32:268–74.CAS 
    PubMed 
    Article 

    Google Scholar 
    Kalyaanamoorthy S, Minh BQ, Wong TK, Von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14:587–9.CAS 
    PubMed 
    PubMed Central 
    Article 

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

    Google Scholar 
    Hoang DT, Chernomor O, Von Haeseler A, Minh BQ, Vinh LS. UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol. 2018;35:518–22.CAS 
    PubMed 
    Article 

    Google Scholar 
    Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 2019;47:W256–9.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19:455–77.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rodriguez-R LM, Gunturu S, Harvey WT, Rosselló-Mora R, Tiedje JM, Cole JR, et al. The Microbial Genomes Atlas (MiGA) webserver: taxonomic and gene diversity analysis of Archaea and Bacteria at the whole genome level. Nucl Acids Res. 2018;46:W282–8.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun. 2018;9:1–8.Article 

    Google Scholar 
    Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068–9.CAS 
    PubMed 
    Article 

    Google Scholar 
    Noble RT, Fuhrman JA. Use of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria. Aquat Microb Ecol. 1998;14:113–8.Article 

    Google Scholar 
    Alcamán-Arias ME, Fuentes-Alburquenque S, Vergara-Barros P, Cifuentes-Anticevic J, Verdugo J, Polz M, et al. Coastal bacterial community response to glacier melting in the Western Antarctic Peninsula. Microorganisms. 2021;9:88.PubMed Central 
    Article 

    Google Scholar 
    Bowman JP, Gosink JJ, McCAMMON SA, Lewis TE, Nichols DS, Nichols PD, et al. Colwellia demingiae sp. nov., Colwellia hornerae sp. nov., Colwellia rossensis sp. nov. and Colwellia psychrotropica sp. nov.: psychrophilic Antarctic species with the ability to synthesize docosahexaenoic acid (22: ω63). Int J Syst Evol Microbiol. 1998;48:1171–80.CAS 

    Google Scholar 
    Reisch CR, Moran MA, Whitman WB. Bacterial catabolism of dimethylsulfoniopropionate (DMSP). Front Microbiol. 2011;2:172.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Diaz J, Ingall E, Benitez-Nelson C, Paterson D, de Jonge MD, McNulty I, et al. Marine polyphosphate: a key player in geologic phosphorus sequestration. Science. 2008;320:652–5.CAS 
    PubMed 
    Article 

    Google Scholar 
    Nichols CM, Bowman JP, Guezennec J. Olleya marilimosa gen. nov., sp. nov., an exopolysaccharide-producing marine bacterium from the family Flavobacteriaceae, isolated from the Southern Ocean. Int J Syst Evol Microbiol. 2005;55:1557–61.CAS 
    PubMed 
    Article 

    Google Scholar 
    von Scheibner M, Sommer U, Jürgens K. Tight coupling of Glaciecola spp. and diatoms during cold-water Phytoplankton spring blooms. Front Microbiol. 2017;8:27.Holmstrom C, Kjelleberg S. Marine Pseudoalteromonas species are associated with higher organisms and produce biologically active extracellular agents. FEMS Microbiol Ecol. 1999;30:285–93.CAS 
    PubMed 
    Article 

    Google Scholar 
    Methe BA, Nelson KE, Deming JW, Momen B, Melamud E, Zhang X, et al. The psychrophilic lifestyle as revealed by the genome sequence of Colwellia psychrerythraea 34H through genomic and proteomic analyses. Proc Natl Acad Sci. 2005;102:10913–8.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kirchman DL. The ecology of Cytophaga–Flavobacteria in aquatic environments. FEMS Microbiol Ecol. 2002;39:91–100.CAS 
    PubMed 

    Google Scholar 
    Hong Z, Lai Q, Luo Q, Jiang S, Zhu R, Liang J, et al. Sulfitobacter pseudonitzschiae sp. nov., isolated from the toxic marine diatom Pseudo-nitzschia multiseries. Int J Syst Evol Microbiol. 2015;65:95–100.CAS 
    PubMed 
    Article 

    Google Scholar 
    Brussaard CPD, Riegman R. Influence of bacteria on phytoplankton cell mortality with phosphorus or nitrogen as the algal-growth-limiting nutrient. Aqua Microb Ecol. 1998;14:271–80.Article 

    Google Scholar 
    Cohen NR, A. Ellis K, Burns WG, Lampe RH, Schuback N, Johnson Z, et al. Iron and vitamin interactions in marine diatom isolates and natural assemblages of the Northeast Pacific Ocean. Limnol Oceanogr. 2017;62:2076–96.CAS 
    Article 

    Google Scholar 
    Hunken M, Harder J, Kirst G. Epiphytic bacteria on the Antarctic ice diatom Amphiprora kufferathii Manguin cleave hydrogen peroxide produced during algal photosynthesis. Plant Biol. 2008;10:519–26.CAS 
    PubMed 
    Article 

    Google Scholar 
    Gourinchas G, Etzl S, Winkler A. Bacteriophytochromes–from informative model systems of phytochrome function to powerful tools in cell biology. Curr Opin Struct Biol. 2019;57:72–83.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Gourion B, Rossignol M, Vorholt JA. A proteomic study of Methylobacterium extorquens reveals a response regulator essential for epiphytic growth. Proc Natl Acad Sci. 2006;103:13186–91.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Mukherjee S, Bassler BL. Bacterial quorum sensing in complex and dynamically changing environments. Nat Rev Microbiol. 2019;17:371–82.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Dong YH, Zhang LH. Quorum sensing and quorum-quenching enzymes. J Microbiol. 2005;43:101–9.CAS 
    PubMed 

    Google Scholar 
    Núñez-Montero K, Barrientos L. Advances in Antarctic research for antimicrobial discovery: a comprehensive narrative review of bacteria from Antarctic environments as potential sources of novel antibiotic compounds against human pathogens and microorganisms of industrial importance. Antibiotics. 2018;7:90.Kieft B, Li Z, Bryson S, Hettich RL, Pan C, Mayali X, et al. Phytoplankton exudates and lysates support distinct microbial consortia with specialized metabolic and ecophysiological traits. Proc Natl Acad Sci. 2021;118:e2101178118.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Maranger R, Bird DF. Viral abundance in aquatic systems: a comparison between marine and fresh waters. Mar Ecol Prog Ser. 1995;121:217–26.Article 

    Google Scholar 
    Sharpe GC, Gifford SM, Septer AN. A model roseobacter, Ruegeria pomeroyi DSS-3, employs a diffusible killing mechanism to eliminate competitors. Msystems. 2020;5:e00443–20.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Cude WN, Mooney J, Tavanaei AA, Hadden MK, Frank AM, Gulvik CA, et al. Production of the antimicrobial secondary metabolite indigoidine contributes to competitive surface colonization by the marine roseobacter Phaeobacter sp. strain Y4I. Appl Environ Microbiol. 2012;78:4771–80.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Long RA, Rowley DC, Zamora E, Liu J, Bartlett DH, Azam F. Antagonistic interactions among marine bacteria impede the proliferation of Vibrio cholerae. Appl Environ Microbiol. 2005;71:8531–6.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bruhn JB, Gram L, Belas R. Production of antibacterial compounds and biofilm formation by Roseobacter species are influenced by culture conditions. Appl Environ Microbiol. 2007;73:442–50.CAS 
    PubMed 
    Article 

    Google Scholar 
    Gromek SM, Suria AM, Fullmer MS, Garcia JL, Gogarten JP, Nyholm SV, et al. Leisingera sp. JC1, a bacterial isolate from Hawaiian bobtail squid eggs, produces indigoidine and differentially inhibits vibrios. Front Microbiol. 2016;7:1342.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Sharifah EN, Eguchi M. The phytoplankton Nannochloropsis oculata enhances the ability of Roseobacter clade bacteria to inhibit the growth of fish pathogen Vibrio anguillarum. PLoS One. 2011;6:e26756.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kerwin AH, Gromek SM, Suria AM, Samples RM, Deoss DJ, O’Donnell K, et al. Shielding the next generation: symbiotic bacteria from a reproductive organ protect bobtail squid eggs from fungal fouling. MBio. 2019;10:e02376–19.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Tonelli M, Signori CN, Bendia A, Neiva J, Ferrero B, Pellizari V, et al. Climate projections for the southern ocean reveal impacts in the marine microbial communities following increases in sea surface temperature. Front Mar Sci. 2021;8:636226.Andrew SM, Morell HT, Strzepek RF, Boyd PW, Ellwood MJ. Iron availability influences the tolerance of southern ocean phytoplankton to warming and elevated irradiance. Front Mar Sci. 2019;6:681.Andrew SM, Strzepek RF, Branson O, Ellwood MJ. Ocean acidification reduces the growth of two Southern Ocean phytoplankton. Mar Ecol Prog Ser. 2022;682:51–64.CAS 
    Article 

    Google Scholar 
    Blin K, Shaw S, Kloosterman AM, Charlop-Powers Z, van Weezel GP, Medema MH, et al. antiSMASH 6.0: improving cluster detection and comparison capabilities. Nucl Acids Res. 2021;49:W29–35.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ferrer-González FX, Widner B, Holderman NR, Glushka J, Edison AS, Kujawinski EB, et al. Resource partitioning of phytoplankton metabolites that support bacterial heterotrophy. ISME J. 2021;15:762–73.PubMed 
    Article 

    Google Scholar  More

  • in

    Defending Earth’s terrestrial microbiome

    Mora, C., Tittensor, D. P., Adl, S., Simpson, A. G. B. & Worm, B. How many species are there on earth and in the ocean? PLoS Biol. 9, e1001127 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Costello, M. J., May, R. M. & Stork, N. E. Can we name earth’s species before they go extinct? Science 339, 413–416 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Corlett, R. T. Plant diversity in a changing world: status, trends, and conservation needs. Plant Divers. 38, 10–16 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Baldrian, P., Větrovský, T., Lepinay, C. & Kohout, P. High-throughput sequencing view on the magnitude of global fungal diversity. Fungal Divers. 114, 539–547 (2022).CAS 
    Article 

    Google Scholar 
    Taylor, D. L. et al. A first comprehensive census of fungi in soil reveals both hyperdiversity and fine-scale niche partitioning. Ecol. Monogr. 84, 3–20 (2014).Article 

    Google Scholar 
    Locey, K. J. & Lennon, J. T. Scaling laws predict global microbial diversity. Proc. Natl Acad. Sci. USA 113, 5970–5975 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Schopf, J. W. Disparate rates, differing fates: tempo and mode of evolution changed from the Precambrian to the Phanerozoic. Proc. Natl Acad. Sci. USA 91, 6735–6742 (1994).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Seager, S., Huang, J., Petkowski, J. J. & Pajusalu, M. Laboratory studies on the viability of life in H2-dominated exoplanet atmospheres. Nat. Astron. 4, 802–806 (2020).Article 

    Google Scholar 
    Halme, P., Holec, J. & Heilmann-Clausen, J. The history and future of fungi as biodiversity surrogates in forests. Fungal Ecol. 27, 193–201 (2017).Article 

    Google Scholar 
    Arnolds, E. Decline of ectomycorrhizal fungi in Europe. Agric. Ecosyst. Environ. 35, 209–244 (1991).Article 

    Google Scholar 
    Boddy, L. in The Fungi (eds Watkinson, S. C. et al.) 361–400 (Elsevier, 2016); https://doi.org/10.1016/B978-0-12-382034-1.00011-6Zimmerman, M. The mushroom message. Sun 11A (1992).Bader, P., Jansson, S. & Jonsson, B. G. Wood-inhabiting fungi and substratum decline in selectively logged boreal spruce forests. Biol. Conserv. 72, 355–362 (1995).Article 

    Google Scholar 
    Weinbauer, M. G. & Rassoulzadegan, F. Extinction of microbes: evidence and potential consequences. Endanger. Species Res. 3, 205–215 (2007).Article 

    Google Scholar 
    Chomicki, G., Kiers, E. T. & Renner, S. S. The evolution of mutualistic dependence. Annu. Rev. Ecol. Evol. Syst. 51, 409–432 (2020).Article 

    Google Scholar 
    Blaser, M. J. The theory of disappearing microbiota and the epidemics of chronic diseases. Nat. Rev. Immunol. 17, 461–463 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Carthey, A. J., Blumstein, D. T., Gallagher, R. V., Tetu, S. G. & Gillings, M. R. Conserving the holobiont. Funct. Ecol. 34, 764–776 (2020).Article 

    Google Scholar 
    Schapheer, C., Pellens, R. & Scherson, R. Arthropod-microbiota integration: its importance for ecosystem conservation. Front. Microbiol. 12, 2094 (2021).Article 

    Google Scholar 
    Zhou, Z., Wang, C. & Luo, Y. Meta-analysis of the impacts of global change factors on soil microbial diversity and functionality. Nat. Commun. 11, 3072 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Anthony, M. A., Stinson, K. A., Moore, J. A. M. & Frey, S. D. Plant invasion impacts on fungal community structure and function depend on soil warming and nitrogen enrichment. Oecologia 194, 659–672 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lilleskov, E., Hobbie, E. A. & Horton, T. Conservation of ectomycorrhizal fungi: exploring the linkages between functional and taxonomic responses to anthropogenic N deposition. Fungal Ecol. 4, 174–183 (2011).Article 

    Google Scholar 
    Gibbons, S. M. et al. Invasive plants rapidly reshape soil properties in a grassland ecosystem. mSystems 2, e00178-16 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rillig, M. C. et al. The role of multiple global change factors in driving soil functions and microbial biodiversity. Science 366, 886–890 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Certini, G., Moya, D., Lucas-Borja, M. E. & Mastrolonardo, G. The impact of fire on soil-dwelling biota: a review. For. Ecol. Manage. 488, 118989 (2021).Article 

    Google Scholar 
    Caruso, T., Hempel, S., Powell, J. R., Barto, E. K. & Rillig, M. C. Compositional divergence and convergence in arbuscular mycorrhizal fungal communities. Ecology 93, 1115–1124 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Anthony, M., Frey, S. & Stinson, K. Fungal community homogenization, shift in dominant trophic guild, and appearance of novel taxa with biotic invasion. Ecosphere 8, e01951 (2017).Article 

    Google Scholar 
    Guerra, C. A. et al. Global projections of the soil microbiome in the Anthropocene. Glob. Ecol. Biogeogr. 30, 987–999 (2021).PubMed 
    Article 

    Google Scholar 
    Enright, D. J., Frangioso, K. M., Isobe, K., Rizzo, D. M. & Glassman, S. I. Mega‐fire in redwood tanoak forest reduces bacterial and fungal richness and selects for pyrophilous taxa that are phylogenetically conserved. Mol. Ecol. 31, 2475–2493 (2022).CAS 
    PubMed 
    Article 

    Google Scholar 
    Anthony, M. A. et al. Forest tree growth is linked to mycorrhizal fungal composition and function across Europe. ISME J. 16, 1327–1336 (2022).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Crowther, T. W. et al. The global soil community and its influence on biogeochemistry. Science 365, eaav0550 (2019).CAS 
    PubMed 
    Article 

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

    Google Scholar 
    Novacek, M. J. & Cleland, E. E. The current biodiversity extinction event: scenarios for mitigation and recovery. Proc. Natl Acad. Sci. USA 98, 5466–5470 (2001).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Guerra, C. A. et al. Tracking, targeting, and conserving soil biodiversity. Science 371, 239–241 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Guerra, C. A. et al. Blind spots in global soil biodiversity and ecosystem function research. Nat. Commun. 11, 3870 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Cameron, E. K. et al. Global mismatches in aboveground and belowground biodiversity. Conserv. Biol. 33, 1187–1192 (2019).PubMed 
    Article 

    Google Scholar 
    Tedersoo, L. et al. Global diversity and geography of soil fungi. Science 346, 1256688 (2014).PubMed 
    Article 

    Google Scholar 
    Bahram, M. et al. Structure and function of the global topsoil microbiome. Nature 560, 233–237 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Delgado-Baquerizo, M. et al. A global atlas of the dominant bacteria found in soil. Science 359, 320–325 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Peixoto, R. S. et al. Harnessing the microbiome to prevent global biodiversity loss. Nat. Microbiol. https://doi.org/10.1038/s41564-022-01173-1 (2022).Box, G. E. P. & Draper, N. R. Empirical Model-building and Response Surfaces (Wiley, 1987).Box, G. E. P., Hunter, W. G. & Hunter, J. S. Statistics for Experimenters: an Introduction to Design, Data Analysis, and Model Building (Wiley, 1978).Kothamasi, D., Spurlock, M. & Kiers, E. T. Agricultural microbial resources: private property or global commons? Nat. Biotechnol. 29, 1091–1093 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    Davison, J. et al. Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349, 970–973 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    van der Linde, S. et al. Environment and host as large-scale controls of ectomycorrhizal fungi. Nature 558, 243–248 (2018).PubMed 
    Article 

    Google Scholar 
    Davison, J. et al. Temperature and pH define the realised niche space of arbuscular mycorrhizal fungi. New Phytol. 231, 763–776 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Ramirez, K. S. et al. Detecting macroecological patterns in bacterial communities across independent studies of global soils. Nat. Microbiol. 3, 189–196 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Wild, S. Quest to map Africa’s soil microbiome begins. Nature 539, 152 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bissett, A. et al. Introducing BASE: the Biomes of Australian Soil Environments soil microbial diversity database. GigaScience 5, 21 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Pan, K., Guo, Z. & Liu, J. Building and materializing of China Soil Microbiome Data Platform. Acta Pedol. Sin. 56, 1023–1033 (2019).
    Google Scholar 
    Orgiazzi, A., Ballabio, C., Panagos, P., Jones, A. & Fernández‐Ugalde, O. LUCAS Soil, the largest expandable soil dataset for Europe: a review. Eur. J. Soil Sci. 69, 140–153 (2018).Article 

    Google Scholar 
    Hinckley, E. S. et al. The soil and plant biogeochemistry sampling design for The National Ecological Observatory Network. Ecosphere 7, e01234 (2016).Article 

    Google Scholar 
    Větrovský, T. et al. GlobalFungi, a global database of fungal occurrences from high-throughput-sequencing metabarcoding studies. Sci. Data 7, 228 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Jackson, F. Sustainable agriculture and a low carbon future: are we missing out on mycelium? Forbes https://www.forbes.com/sites/feliciajackson/2021/12/02/sustainable-agriculture-and-a-low-carbon-future-are-we-missing-out-on-mycelium/?sh=3dc1a6d076ed (2021).Gilbert, J. A., Jansson, J. K. & Knight, R. The Earth Microbiome project: successes and aspirations. BMC Biol. 12, 69 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Fedrowitz, K. et al. Can retention forestry help conserve biodiversity? A meta‐analysis. J. Appl. Ecol. 51, 1669–1679 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Schmidt, R., Mitchell, J. & Scow, K. Cover cropping and no-till increase diversity and symbiotroph:saprotroph ratios of soil fungal communities. Soil Biol. Biochem. 129, 99–109 (2019).CAS 
    Article 

    Google Scholar 
    Status of the World’s Soil Resources: Main Report (FAO, 2015).Aronson, J., Goodwin, N., Orlando, L., Eisenberg, C. & Cross, A. T. A world of possibilities: six restoration strategies to support the United Nation’s Decade on Ecosystem Restoration. Restor. Ecol. 28, 730–736 (2020).Article 

    Google Scholar 
    Seymour, F. Seeing the forests as well as the (trillion) trees in corporate climate strategies. One Earth 2, 390–393 (2020).Article 

    Google Scholar 
    Dinerstein, E. et al. A global deal for nature: guiding principles, milestones, and targets. Sci. Adv. 5, eaaw2869 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Philipson, C. D. et al. Active restoration accelerates the carbon recovery of human-modified tropical forests. Science 369, 838–841 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Coleman, E. A. et al. Limited effects of tree planting on forest canopy cover and rural livelihoods in Northern India. Nat. Sustain. 4, 997–1004 (2021).Article 

    Google Scholar 
    Neuenkamp, L., Prober, S. M., Price, J. N., Zobel, M. & Standish, R. J. Benefits of mycorrhizal inoculation to ecological restoration depend on plant functional type, restoration context and time. Fungal Ecol. 40, 140–149 (2019).Article 

    Google Scholar 
    Koziol, L. et al. Manipulating plant microbiomes in the field: native mycorrhizae advance plant succession and improve native plant restoration. J. Appl. Ecol. https://doi.org/10.1111/1365-2664.14036 (2021).Wubs, E. R. J., van der Putten, W. H., Bosch, M. & Bezemer, T. M. Soil inoculation steers restoration of terrestrial ecosystems. Nat. Plants 2, 16107 (2016).PubMed 
    Article 

    Google Scholar 
    Bever, J. & Schultz, P. Prairie mycorrhizal fungi inoculant may increase native plant diversity on restored sites (Illinois). Ecol. Restor. 21, 311–312 (2003).
    Google Scholar 
    Vahter, T. et al. Co-introduction of native mycorrhizal fungi and plant seeds accelerates restoration of post-mining landscapes. J. Appl. Ecol. 57, 1741–1751 (2020).CAS 
    Article 

    Google Scholar 
    Egan, C. P. et al. Restoration of the mycobiome of the endangered Hawaiian mint Phyllostegia kaalaensis increases its resistance to a common powdery mildew. Fungal Ecol. 52, 101070 (2021).Article 

    Google Scholar 
    Wubs, E. R. J. et al. Single introductions of soil biota and plants generate long‐term legacies in soil and plant community assembly. Ecol. Lett. 22, 1145–1151 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Abrego, N. et al. Reintroduction of threatened fungal species via inoculation. Biol. Conserv. 203, 120–124 (2016).Article 

    Google Scholar 
    Salomon, M. J. et al. Global evaluation of commercial arbuscular mycorrhizal inoculants under greenhouse and field conditions. Appl. Soil Ecol. 169, 104225 (2022).Article 

    Google Scholar 
    Maltz, M. R. & Treseder, K. K. Sources of inocula influence mycorrhizal colonization of plants in restoration projects: a meta-analysis: mycorrhizal inoculation in restoration. Restor. Ecol. 23, 625–634 (2015).Article 

    Google Scholar 
    Busby, P. E., Newcombe, G., Neat, A. S. & Averill, C. Facilitating reforestation through the plant microbiome: perspectives from the phyllosphere. Annu. Rev. Phytopathol. https://doi.org/10.1146/annurev-phyto-021320-010717 (2022).van der Heijden, M. G. A., Martin, F. M., Selosse, M.-A. & Sanders, I. R. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol. 205, 1406–1423 (2015).PubMed 
    Article 

    Google Scholar 
    Crowther, T. W. et al. Predicting the responsiveness of soil biodiversity to deforestation: a cross-biome study. Glob. Change Biol. 20, 2983–2994 (2014).Article 

    Google Scholar 
    Lilleskov, E. A., Kuyper, T. W., Bidartondo, M. I. & Hobbie, E. A. Atmospheric nitrogen deposition impacts on the structure and function of forest mycorrhizal communities: a review. Environ. Pollut. 246, 148–162 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Smith, G. R., Steidinger, B. S., Bruns, T. D. & Peay, K. G. Competition–colonization tradeoffs structure fungal diversity. ISME J. 12, 1758–1767 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ceballos, I. et al. The in vitro mass-produced model mycorrhizal fungus, Rhizophagus irregularis, significantly increases yields of the globally important food security crop cassava. PLoS ONE 8, e70633 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Buysens, C., César, V., Ferrais, F., de Boulois, H. D. & Declerck, S. Inoculation of Medicago sativa cover crop with Rhizophagus irregularis and Trichoderma harzianum increases the yield of subsequently-grown potato under low nutrient conditions. Appl. Soil Ecol. 105, 137–143 (2016).Article 

    Google Scholar 
    Antunes, P. M. et al. Influence of commercial inoculation with Glomus intraradices on the structure and functioning of an AM fungal community from an agricultural site. Plant Soil 317, 257–266 (2009).CAS 
    Article 

    Google Scholar 
    Emam, T. Local soil, but not commercial AMF inoculum, increases native and non‐native grass growth at a mine restoration site. Restor. Ecol. 24, 35–44 (2016).Article 

    Google Scholar 
    Hoeksema, J. D. et al. A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol. Lett. 13, 394–407 (2010).PubMed 
    Article 

    Google Scholar 
    Policelli, N., Horton, T. R., Hudon, A. T., Patterson, T. R. & Bhatnagar, J. M. Back to roots: the role of ectomycorrhizal fungi in boreal and temperate forest restoration. Front. For. Glob. Change 3, 97 (2020).Article 

    Google Scholar 
    Hoeksema, J. D. et al. Ectomycorrhizal plant-fungal co-invasions as natural experiments for connecting plant and fungal traits to their ecosystem consequences. Front. Glob. Change 3, 84 (2020).Article 

    Google Scholar 
    Land Use Statistics and Indicators. Global, Regional and Country Trends 1990– 2019 FAOSTAT Analytical Brief Series No. 28 (FAO, 2021).Stewart, W. M., Dibb, D. W., Johnston, A. E. & Smyth, T. J. The contribution of commercial fertilizer nutrients to food production. Agron. J. 97, 1–6 (2005).Article 

    Google Scholar 
    Harlander, S. K. The evolution of modern agriculture and its future with biotechnology. J. Am. Coll. Nutr. 21, 161S–165S (2002).PubMed 
    Article 

    Google Scholar 
    Cooper, J. & Dobson, H. The benefits of pesticides to mankind and the environment. Crop Prot. 26, 1337–1348 (2007).CAS 
    Article 

    Google Scholar 
    Zsögön, A., Peres, L. E. P., Xiao, Y., Yan, J. & Fernie, A. R. Enhancing crop diversity for food security in the face of climate uncertainty. Plant J. https://doi.org/10.1111/tpj.15626 (2021).IPCC Climate Change 2013: The Physical Science Basis (eds Stocker, T. F. et al.) (Cambridge Univ. Press, 2013).McDonald, B. A. & Stukenbrock, E. H. Rapid emergence of pathogens in agro-ecosystems: global threats to agricultural sustainability and food security. Phil. Trans. R. Soc. Lond. B 371, 20160026 (2016).Article 

    Google Scholar 
    Avelino, J. et al. The coffee rust crises in Colombia and Central America (2008–2013): impacts, plausible causes and proposed solutions. Food Sec. 7, 303–321 (2015).Article 

    Google Scholar 
    Goss, E. M. et al. The Irish potato famine pathogen Phytophthora infestans originated in central Mexico rather than the Andes. Proc. Natl Acad. Sci. USA 111, 8791–8796 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ploetz, R. C. Panama disease: a classic and destructive disease of banana. Plant Health Prog. https://doi.org/10.1094/PHP-2000-1204-01-HM (2000).Craven, D. et al. Multiple facets of biodiversity drive the diversity–stability relationship. Nat. Ecol. Evol. 2, 1579–1587 (2018).PubMed 
    Article 

    Google Scholar 
    Thibaut, L. M. & Connolly, S. R. Understanding diversity–stability relationships: towards a unified model of portfolio effects. Ecol. Lett. 16, 140–150 (2013).PubMed 
    Article 

    Google Scholar 
    Isbell, F. et al. Biodiversity increases the resistance of ecosystem productivity to climate extremes. Nature 526, 574–577 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Prieto, I. et al. Complementary effects of species and genetic diversity on productivity and stability of sown grasslands. Nat. Plants 1, 15033 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Liang, J. et al. Positive biodiversity-productivity relationship predominant in global forests. Science 354, aaf8957 (2016).PubMed 
    Article 

    Google Scholar 
    Cornell, C. et al. Do bioinoculants affect resident microbial communities? A meta-analysis. Front. Agron. 3, 753474 (2021).Article 

    Google Scholar 
    Manning, L. Groundwork BioAg raises $11m to expand mycorrhizal inputs business. AgFunder Network https://agfundernews.com/groundwork-bioag-raises-11m-to-expand-mycorrhizal-inputs-business (2021).Egidi, E. et al. A few Ascomycota taxa dominate soil fungal communities worldwide. Nat. Commun. 10, 2369 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Olle, M. & Williams, I. H. Effective microorganisms and their influence on vegetable production—a review. J. Hortic. Sci. Biotechnol. 88, 380–386 (2013).Article 

    Google Scholar 
    Mayer, J., Scheid, S., Widmer, F., Fließbach, A. & Oberholzer, H.-R. How effective are ‘Effective microorganisms® (EM)’? Results from a field study in temperate climate. Appl. Soil Ecol. 46, 230–239 (2010).Article 

    Google Scholar 
    Kodippili, K. P. A. N. & Nimalan, J. Effect of homemade effective microorganisms on the growth and yield of chilli (Capsicum annuum) MI-2. AGRIEAST J. Agric. Sci. https://doi.org/10.4038/agrieast.v12i2.57 (2018).de Araujo Avila, G. M., Gabardo, G., Clock, D. C. & de Lima Junior, O. S. Use of efficient microorganisms in agriculture. Res. Soc. Dev. https://doi.org/10.33448/rsd-v10i8.17515 (2021).Saleem, M., Hu, J. & Jousset, A. More than the sum of its parts: microbiome biodiversity as a driver of plant growth and soil health. Annu. Rev. Ecol. Evol. Syst. 50, 145–168 (2019).Article 

    Google Scholar 
    Bradford, M. A. et al. Thermal adaptation of soil microbial respiration to elevated temperature. Ecol. Lett. 11, 1316–1327 (2008).PubMed 
    Article 

    Google Scholar 
    Romero-Olivares, A. L., Allison, S. D. & Treseder, K. K. Soil microbes and their response to experimental warming over time: a meta-analysis of field studies. Soil Biol. Biochem. 107, 32–40 (2017).CAS 
    Article 

    Google Scholar 
    Klironomos, J. N. Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84, 2292–2301 (2003).Article 

    Google Scholar 
    Veen, C. G. F., Snoek, B. L., Bakx-Schotman, T., Wardle, D. A. & van der Putten, W. H. Relationships between fungal community composition in decomposing leaf litter and home-field advantage effects. Funct. Ecol. 33, 1524–1535 (2019).Article 

    Google Scholar 
    Wang, Q., Zhong, M. & He, T. Home-field advantage of litter decomposition and nitrogen release in forest ecosystems. Biol. Fertil. Soils 49, 427–434 (2013).CAS 
    Article 

    Google Scholar 
    Hawkes, C. V., Waring, B. G., Rocca, J. D. & Kivlin, S. N. Historical climate controls soil respiration responses to current soil moisture. Proc. Natl Acad. Sci. USA 114, 6322–6327 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Morriën, E. et al. Soil networks become more connected and take up more carbon as nature restoration progresses. Nat. Commun. 8, 14349 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Wagg, C., Bender, S. F., Widmer, F. & van der Heijden, M. G. A. Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc. Natl Acad. Sci. USA 111, 5266–5270 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Wittebolle, L. et al. Initial community evenness favours functionality under selective stress. Nature 458, 623–626 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    de Graaff, M.-A., Adkins, J., Kardol, P. & Throop, H. A meta-analysis of soil biodiversity impacts on the carbon cycle. Soil 1, 257–271 (2015).Article 

    Google Scholar 
    Gao, J. et al. Assessing the effect of leaf litter diversity on the decomposition and associated diversity of fungal assemblages. Forests 6, 2371–2386 (2015).Article 

    Google Scholar 
    Selosse, M.-A., Bouchard, D., Martin, F. & Tacon, F. L. Effect of Laccaria bicolor strains inoculated on Douglas-fir (Pseudotsuga menziesii) several years after nursery inoculation. Can. J. Res. 30, 360–371 (2000).Article 

    Google Scholar 
    Banerjee, S. et al. Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots. ISME J. 13, 1722–1736 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

  • in

    Unravelling the interplay of ecological processes structuring the bacterial rare biosphere

    Pedros-Alio C. The rare bacterial biosphere. Ann Rev Mar Sci. 2012;4:449–66. https://doi.org/10.1146/annurev-marine-120710-100948.Article 
    PubMed 

    Google Scholar 
    Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR, et al. Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci. 2006;103:12115–20. https://doi.org/10.1073/pnas.0605127103.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Hausmann B, Pelikan C, Rattei T, Loy A, Pester M. Long-term transcriptional activity at zero growth of a cosmopolitan rare biosphere member. mBio. 2019;10:e02189–18. https://doi.org/10.1128/mBio.02189-18.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Pester M, Bittner N, Deevong P, Wagner M, Loy AA. ‘Rare biosphere’microorganism contributes to sulfate reduction in a peatland. ISME J. 2010;4:1591–602.Article 

    Google Scholar 
    Rivett DW, Bell T. Abundance determines the functional role of bacterial phylotypes in complex communities. Nat Microbiol. 2018;3:767–72. https://doi.org/10.1038/s41564-018-0180-0.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    van Elsas JD, Chiurazzi M, Mallon CA, Elhottova D, Kristufek V, Salles JF. Microbial diversity determines the invasion of soil by a bacterial pathogen. Proc Natl Acad Sci USA. 2012;109:1159–64. https://doi.org/10.1073/pnas.1109326109.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Magurran AE, Henderson PA. Explaining the excess of rare species in natural species abundance distributions. Nature. 2003;422:714–6.Article 

    Google Scholar 
    Rabinowitz D, Rapp JK, Dixon PM. Competitive abilities of sparse grass species: means of persistence or cause of abundance. Ecology. 1984;65:1144–54. https://doi.org/10.2307/1938322.Article 

    Google Scholar 
    Reinhardt K, Köhler G, Maas S, Detzel P. Low dispersal ability and habitat specificity promote extinctions in rare but not in widespread species: the Orthoptera of Germany. Ecography. 2005;28:593–602. https://doi.org/10.1111/j.2005.0906-7590.04285.x.Article 

    Google Scholar 
    Yenni G, Adler PB, Ernest S. Strong self-limitation promotes the persistence of rare species. Ecology. 2012;93:456–61.Article 

    Google Scholar 
    Jousset A, Bienhold C, Chatzinotas A, Gallien L, Gobet A, Kurm V, et al. Where less may be more: how the rare biosphere pulls ecosystems strings. The ISME J. 2017;11:853–62. https://doi.org/10.1038/ismej.2016.174.Article 
    PubMed 

    Google Scholar 
    Thingstad TF. Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol Oceanogr. 2000;45:1320–8. https://doi.org/10.4319/lo.2000.45.6.1320.Article 

    Google Scholar 
    Szekely AJ, Langenheder S. The importance of species sorting differs between habitat generalists and specialists in bacterial communities. FEMS Microbiol Ecol. 2014;87:102–12. https://doi.org/10.1111/1574-6941.12195.Article 
    PubMed 

    Google Scholar 
    Mo Y, Zhang W, Yang J, Lin Y, Yu Z, Lin S. Biogeographic patterns of abundant and rare bacterioplankton in three subtropical bays resulting from selective and neutral processes. ISME J. 2018;12:2198–210. https://doi.org/10.1038/s41396-018-0153-6.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Nemergut DR, Schmidt SK, Fukami T, O’Neill SP, Bilinski TM, Stanish LF, et al. Patterns and processes of microbial community assembly. Microbiol Mol Biology Rev. 2013;77:342–56. https://doi.org/10.1128/MMBR.00051-12.Article 

    Google Scholar 
    Vellend M. Conceptual synthesis in community ecology. Q Rev Biol. 2010;85:183–206. https://doi.org/10.1086/652373.Article 
    PubMed 

    Google Scholar 
    Vellend M The Theory of Ecological Communities. Princeton University Pres. 2016:61-7.Jia X, Dini-Andreote F, Falcao Salles J. Community assembly processes of the microbial rare biosphere. Trends Microbiol. 2018;26:738–47. https://doi.org/10.1016/j.tim.2018.02.011.Article 
    PubMed 

    Google Scholar 
    Stegen JC, Lin X, Fredrickson JK, Chen X, Kennedy DW, Murray CJ, et al. Quantifying community assembly processes and identifying features that impose them. ISME J. 2013;7:2069–79. https://doi.org/10.1038/ismej.2013.93.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Stegen JC, Lin X, Fredrickson JK, Konopka AE. Estimating and mapping ecological processes influencing microbial community assembly. Front Microbiol. 2015;6:https://doi.org/10.3389/fmicb.2015.00370.Webb CO, Ackerly DD, McPeek MA, Donoghue MJ. Phylogenies and community ecology. Ann Rev Ecol Syst. 2002;33:475–505. https://doi.org/10.1146/annurev.ecolsys.33.010802.150448.Article 

    Google Scholar 
    Lynch MDJ, Neufeld JD. Ecology and exploration of the rare biosphere. Nat Rev Micro. 2015;13:217–29. https://doi.org/10.1038/nrmicro3400.Article 

    Google Scholar 
    Dini-Andreote F, Stegen JC, van Elsas JD, Salles JF. Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Proc Natl Acad Sci USA. 2015;112:E1326–E32. https://doi.org/10.1073/pnas.1414261112.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Chase JM, Kraft NJB, Smith KG, Vellend M, Inouye BD. Using null models to disentangle variation in community dissimilarity from variation in α-diversity. Ecosphere. 2011;2:art24 https://doi.org/10.1890/es10-00117.1.Article 

    Google Scholar 
    Shade A, Jones SE, Caporaso JG, Handelsman J, Knight R, Fierer N, et al. Conditionally rare taxa disproportionately contribute to temporal changes in microbial diversity. mBio. 2014;5:e01371–14. https://doi.org/10.1128/mBio.01371-14.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Strous M, Heijnen JJ, Kuenen JG, Jetten MSM. The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms. Appl Microbiol Biotechnol. 1998;50:589–96. https://doi.org/10.1007/s002530051340.Article 

    Google Scholar 
    Goldfarb KC, Karaoz U, Hanson CA, Santee CA, Bradford MA, Treseder KK, et al. Differential growth responses of soil bacterial taxa to carbon substrates of varying chemical recalcitrance. Front Microbiol. 2011;2:94. https://doi.org/10.3389/fmicb.2011.00094.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Jia X, Dini-Andreote F, Falcao Salles J. Comparing the influence of assembly processes governing bacterial community succession based on DNA and RNA Data. Microorganisms. 2020;8. https://doi.org/10.3390/microorganisms8060798.Olff H, De Leeuw J, Bakker JP, Platerink RJ, van Wijnen HJ. Vegetation succession and herbivory in a salt marsh: changes induced by sea level rise and silt deposition along an elevational gradient. J Ecol. 1997;85:799–814. https://doi.org/10.2307/2960603.Article 

    Google Scholar 
    Dini-Andreote F, Silva M, Triado-Margarit X, Casamayor EO, van Elsas JD, Salles JF. Dynamics of bacterial community succession in a salt marsh chronosequence: evidences for temporal niche partitioning. ISME J. 2014;8:1989–2001. https://doi.org/10.1038/ismej.2014.54.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Dini-Andreote F, Pylro VS, Baldrian P, van Elsas JD, Salles JF. Ecological succession reveals potential signatures of marine–terrestrial transition in salt marsh fungal communities. ISME J. 2016;10:1984–97.Article 

    Google Scholar 
    Schrama M, Berg MP, Olff H. Ecosystem assembly rules: the interplay of green and brown webs during salt marsh succession. Ecology. 2012;93:2353–64.Article 

    Google Scholar 
    Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci. 2011;108:4516–22. https://doi.org/10.1073/pnas.1000080107.Article 
    PubMed 

    Google Scholar 
    Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 2012;6:1621–4.Article 

    Google Scholar 
    Carini P, Marsden PJ, Leff JW, Morgan EE, Strickland MS, Fierer N. Relic DNA is abundant in soil and obscures estimates of soil microbial diversity. Nat Microbiol. 2016;2:16242. https://doi.org/10.1038/nmicrobiol.2016.242.Article 
    PubMed 

    Google Scholar 
    Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet C, Al-Ghalith GA, et al. QIIME 2: Reproducible, interactive, scalable, and extensible microbiome data science. PeerJ Preprints. 2018;6:e27295v2. https://doi.org/10.7287/peerj.preprints.27295v2.Article 

    Google Scholar 
    Callahan BJ, McMurdie PJ, Holmes SP. Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J. 2017;11:2639–43. https://doi.org/10.1038/ismej.2017.119.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Yilmaz P, Parfrey LW, Yarza P, Gerken J, Pruesse E, Quast C, et al. The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks. Nucleic Acids Res. 2014;42:D643–8. https://doi.org/10.1093/nar/gkt1209.Article 
    PubMed 

    Google Scholar 
    Price MN, Dehal PS, Arkin AP. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol. 2009;26:1641–50.Article 

    Google Scholar 
    R Core Team: R: A language and environment for statistical computing. In. Vienna, Austria: R Foundation for Statistical Computing; 2017.RStudio Team: RStudio: integrated development for R. In., vol. 42. Boston, MA: RStudio, Inc.; 2015.Wickham H. ggplot2: elegant graphics for data analysis. J Stat Softw. 2010;35:65–88.
    Google Scholar 
    Chen H, Boutros PC. VennDiagram: a package for the generation of highly-customizable Venn and Euler diagrams in R. BMC Bioinf. 2011;12:35.Article 

    Google Scholar 
    Dixon P. VEGAN, a package of R functions for community ecology. J Veg Sci. 2003;14:927–30. https://doi.org/10.1111/j.1654-1103.2003.tb02228.x.Article 

    Google Scholar 
    Yamamoto K, Hackley KC, Kelly WR, Panno SV, Sekiguchi Y, Sanford RA, et al. Diversity and geochemical community assembly processes of the living rare biosphere in a sand-and-gravel aquifer ecosystem in the Midwestern United States. Sci Rep. 2019;9. https://doi.org/10.1038/s41598-019-49996-z.Galand PE, Casamayor EO, Kirchman DL, Lovejoy C. Ecology of the rare microbial biosphere of the Arctic Ocean. Proc Natl Acad Sci. 2009;106:22427–32. https://doi.org/10.1073/pnas.0908284106.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Reveillaud J, Maignien L, Murat Eren A, Huber JA, Apprill A, Sogin ML, et al. Host-specificity among abundant and rare taxa in the sponge microbiome. ISME J. 2014;8:1198–209. https://doi.org/10.1038/ismej.2013.227.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Logares R, Audic S, Bass D, Bittner L, Boutte C, Christen R, et al. Patterns of rare and abundant marine microbial eukaryotes. Curr Biol. 2014;24:813–21. https://doi.org/10.1016/j.cub.2014.02.050.Article 
    PubMed 

    Google Scholar 
    Campbell BJ, Yu L, Heidelberg JF, Kirchman DL. Activity of abundant and rare bacteria in a coastal ocean. Proc Natl Acad Sci. 2011;108:12776–81. https://doi.org/10.1073/pnas.1101405108.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Hirsch JE. An index to quantify an individual’s scientific research output. Proc Natl Acad Sci USA. 2005;102:16569. https://doi.org/10.1073/pnas.0507655102.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Haegeman B, Hamelin J, Moriarty J, Neal P, Dushoff J, Weitz JS. Robust estimation of microbial diversity in theory and in practice. ISME J. 2013;7:1092–101. https://doi.org/10.1038/ismej.2013.10.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Paradis E, Claude J, Strimmer K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics (Oxford, England). 2004;20:289–90.Article 

    Google Scholar 
    Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, et al. Picante: R tools for integrating phylogenies and ecology. Bioinformatics. 2010;26:1463–4.Article 

    Google Scholar 
    Stegen JC, Lin X, Konopka AE, Fredrickson JK. Stochastic and deterministic assembly processes in subsurface microbial communities. ISME J. 2012;6:1653–64. https://doi.org/10.1038/ismej.2012.22.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Jiao S, Lu Y. Soil pH and temperature regulate assembly processes of abundant and rare bacterial communities in agricultural ecosystems. Environ Microbiol. 2020;22:1052–65. https://doi.org/10.1111/1462-2920.14815.Article 
    PubMed 

    Google Scholar 
    Logares R, Lindström ES, Langenheder S, Logue JB, Paterson H, Laybourn-Parry J, et al. Biogeography of bacterial communities exposed to progressive long-term environmental change. ISME J. 2012;7:937–48. https://doi.org/10.1038/ismej.2012.168.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kurm V, van der Putten WH, Weidner S, Geisen S, Snoek BL, Bakx T, et al. Competition and predation as possible causes of bacterial rarity. Environ Microbiol. 2019;21:1356–68. https://doi.org/10.1111/1462-2920.14569.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Aanderud ZT, Saurey S, Ball BA, Wall DH, Barrett JE, Muscarella ME, et al. Stoichiometric shifts in Soil C:N:P promote bacterial taxa dominance, maintain biodiversity, and deconstruct community assemblages. Front Microbiol. 2018;9:1401 https://doi.org/10.3389/fmicb.2018.01401.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sloan WT, Woodcock S, Lunn M, Head IM, Curtis TP. Modeling taxa-abundance distributions in microbial communities using environmental sequence data. Microb Ecol. 2007;53:443–55. https://doi.org/10.1007/s00248-006-9141-x.Article 
    PubMed 

    Google Scholar 
    Magurran AE, McGill BJ. Biological diversity: frontiers in measurement and assessment. Oxford University Press; 2011.Richter-Heitmann T, Hofner B, Krah FS, Sikorski J, Wust PK, Bunk B, et al. Stochastic dispersal rather than deterministic selection explains the spatio-temporal distribution of soil bacteria in a temperate grassland. Front Microbiol. 2020;11:1391. https://doi.org/10.3389/fmicb.2020.01391.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ivanov II, Honda K. Intestinal commensal microbes as immune modulators. Cell Host Microbe. 2012;12:496–508. https://doi.org/10.1016/j.chom.2012.09.009.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    van Veelen HPJ, Falcao Salles J, Tieleman BI. Multi-level comparisons of cloacal, skin, feather and nest-associated microbiota suggest considerable influence of horizontal acquisition on the microbiota assembly of sympatric woodlarks and skylarks. Microbiome. 2017;5:156. https://doi.org/10.1186/s40168-017-0371-6.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Warmink JA, Nazir R, Corten B, van Elsas JD. Hitchhikers on the fungal highway: The helper effect for bacterial migration via fungal hyphae. Soil Biology Biochem. 2011;43:760–5. https://doi.org/10.1016/j.soilbio.2010.12.009.Article 

    Google Scholar 
    Snell Taylor SJ, Evans BS, White EP, Hurlbert AH. The prevalence and impact of transient species in ecological communities. Ecology. 2018;99:1825–35. https://doi.org/10.1002/ecy.2398.Article 
    PubMed 

    Google Scholar 
    Kurm V, Geisen S, Gera Hol WH. A low proportion of rare bacterial taxa responds to abiotic changes compared with dominant taxa. Environ Microbiol. 2019;21:750–8. https://doi.org/10.1111/1462-2920.14492.Article 
    PubMed 

    Google Scholar 
    Wang Y, Hatt JK, Tsementzi D, Rodriguez RL, Ruiz-Perez CA, Weigand MR, et al. Quantifying the Importance of the Rare Biosphere for Microbial Community Response to Organic Pollutants in a Freshwater Ecosystem. Appl Environ Microbiol. 2017;83:e03321–16. https://doi.org/10.1128/AEM.03321-16.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Cao J, Jia X, Pang S, Hu Y, Li Y, Wang Q. Functional structure, taxonomic composition and the dominant assembly processes of soil prokaryotic community along an altitudinal gradient. Appl Soil Ecol. 2020;155. https://doi.org/10.1016/j.apsoil.2020.103647.Meyer KM, Memiaghe H, Korte L, Kenfack D, Alonso A, Bohannan BJM. Why do microbes exhibit weak biogeographic patterns. ISME J. 2018;12:1404–13. https://doi.org/10.1038/s41396-018-0103-3.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Anderson RE, Sogin ML, Baross JA. Biogeography and ecology of the rare and abundant microbial lineages in deep-sea hydrothermal vents. FEMS Microbiol Ecol. 2015;91:1–11. https://doi.org/10.1093/femsec/fiu016.Article 
    PubMed 

    Google Scholar 
    Mallon CA, Le Roux X, van Doorn GS, Dini-Andreote F, Poly F, Salles JF. The impact of failure: unsuccessful bacterial invasions steer the soil microbial community away from the invader’s niche. ISME J. 2018;12:728–41. https://doi.org/10.1038/s41396-017-0003-y.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Langenheder S, Bulling MT, Solan M, Prosser JI. Bacterial biodiversity-ecosystem functioning relations are modified by environmental complexity. PLoS One. 2010;5:e10834. https://doi.org/10.1371/journal.pone.0010834.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bardgett RD, Van Der Putten WH. Belowground biodiversity and ecosystem functioning. Nature. 2014;515:505.Article 

    Google Scholar 
    Griffiths B, Ritz K, Wheatley R, Kuan H, Boag B, Christensen S, et al. An examination of the biodiversity–ecosystem function relationship in arable soil microbial communities. Soil Biol Biochem. 2001;33:1713–22.Article 

    Google Scholar 
    Hooper DU, Chapin F, Ewel J, Hector A, Inchausti P, Lavorel S, et al. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr. 2005;75:3–35.Article 

    Google Scholar 
    Logares R, Tesson SVM, Canback B, Pontarp M, Hedlund K, Rengefors K. Contrasting prevalence of selection and drift in the community structuring of bacteria and microbial eukaryotes. Environ Microbiol. 2018;20:2231–40. https://doi.org/10.1111/1462-2920.14265.Article 
    PubMed 

    Google Scholar 
    Zhou J, Ning D. Stochastic community assembly: does it matter in microbial ecology? Microbiol Mol Biol Rev. 2017;81:e00002–17.Article 

    Google Scholar 
    Logares R, Deutschmann IM, Junger PC, Giner CR, Krabberod AK, Schmidt TSB, et al. Disentangling the mechanisms shaping the surface ocean microbiota. Microbiome. 2020;8:55. https://doi.org/10.1186/s40168-020-00827-8.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Dini-Andreote F, Brossi MJ, van Elsas JD, Salles JF. Reconstructing the genetic potential of the microbially-mediated nitrogen cycle in a salt marsh ecosystem. Front Microbiol. 2016;7:902. https://doi.org/10.3389/fmicb.2016.00902.Article 
    PubMed 
    PubMed Central 

    Google Scholar  More