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    Sensing whales, storms, ships and earthquakes using an Arctic fibre optic cable

    Howe, B. M. et al. Observing the oceans acoustically. Front. Mar. Sci. 6, 426. https://doi.org/10.3389/fmars.2019.00426 (2019).Article 

    Google Scholar 
    Molenaar, M. M., Hill, D., Webster, P., Fidan, E. & Birch, B. First downhole application of distributed acoustic sensing for hydraulic-fracturing monitoring and diagnostics. SPE Drill. Complet. 27, 32–38. https://doi.org/10.2118/140561-PA (2012).Article 

    Google Scholar 
    Lindsey, N. J. et al. Fiber-optic network observations of earthquake wavefields. Geophys. Res. Lett. 44, 11792–11799. https://doi.org/10.1002/2017GLO75722 (2017).Article 
    ADS 

    Google Scholar 
    Jousset, P. et al. Dynamic strain determination using fibre-optic cables allows imaging of seismological and structural features. Nat. Commun. 9, 1–11. https://doi.org/10.1038/s41467-018-04860-y (2018).Article 
    CAS 

    Google Scholar 
    Ajo-Franklin, J. B. et al. Distributed acoustic sensing using dark fiber for near-surface characterization and broadband seismic event detection. Sci. Rep. 9, 1–14. https://doi.org/10.1038/s41598-018-36675-8 (2019).Article 
    CAS 

    Google Scholar 
    Williams, E. F. et al. Distributed sensing of microseisms and teleseisms with submarine dark fibers. Nat. Commun. 10, 1–11. https://doi.org/10.1038/s41467-019-13262-7 (2019).Article 
    CAS 

    Google Scholar 
    Lindsey, N. J., Dawe, T. C. & Ajo-Franklin, J. B. Illuminating seafloor faults and ocean dynamics with dark fiber distributed acoustic sensing. Science 366, 1103–1107. https://doi.org/10.1126/science.aay5881 (2019).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Sladen, A. et al. Distributed sensing of earthquakes and ocean-solid Earth interactions on seafloor telecom cables. Nat. Commun. 10, 5777. https://doi.org/10.1038/s41467-019-13793-z (2019).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Williams, E. F. et al. Surface gravity wave interferometry and ocean current monitoring with ocean-bottom DAS. J. Geophys. Res. Oceans 127, e2021JC018375. https://doi.org/10.1029/2021JC018375 (2022).Article 
    ADS 

    Google Scholar 
    Zhan, Z. et al. Optical polarization-based seismic and water wave sensing on transoceanic cables. Science 371, 931–936. https://doi.org/10.1126/science.abe6648 (2021).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Waagaard, O. H. et al. Real-time low noise distributed acoustic sensing in 171 km low loss fiber. OSA Contin. 4, 688–701. https://doi.org/10.1364/OSAC.408761 (2021).Article 
    CAS 

    Google Scholar 
    Rivet, D., de Cacqueray, B., Sladen, A., Roques, A. & Calbris, G. Preliminary assessment of ship detection and trajectory evaluation using distributed acoustic sensing on an optical fiber telecom cable. J. Acoust. Soc. Am. 149, 2615–2627. https://doi.org/10.1121/10.0004129 (2021).Article 
    ADS 
    PubMed 

    Google Scholar 
    Taweesintananon, K., Landrø, M., Brenne, J. K. & Haukanes, A. Distributed acoustic sensing for near-surface imaging using submarine telecommunication cable: a case study in the Trondheimsfjord, Norway. Geophysics 86, B303–B320. https://doi.org/10.1190/geo2020-0834.1 (2021).Article 

    Google Scholar 
    Matsumoto, H. et al. Detection of hydroacoustic signals on a fiber-optic submarine cable. Sci. Rep. 11, 2797. https://doi.org/10.1038/s41598-021-82093-8 (2021).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bouffaut, L. et al. Eavesdropping at the speed of light: Distributed acoustic sensing of baleen whales in the Arctic. Front. Mar. Sci. 9, 901348. https://doi.org/10.3389/fmars.2022.901348 (2022).Article 

    Google Scholar 
    Jones, N. The quest for quieter seas. Nature 568, 158–161. https://doi.org/10.1038/d41586-019-01098-6 (2019).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Williams, R. et al. Chronic ocean noise and cetacean population models. J. Cetacean Res. Manag. 21, 85–94. https://doi.org/10.47536/jcrm.v21i1.202 (2020).Article 

    Google Scholar 
    Roman, J. et al. Whales as marine ecosystem engineers. Front. Ecol. Environ. 12, 377–385. https://doi.org/10.1890/130220 (2014).Article 

    Google Scholar 
    Pershing, A. J., Christensen, L. B., Record, N. R., Sherwood, G. D. & Stetson, P. B. The impact of whaling on the ocean carbon cycle: Why bigger was better. PLoS ONE 5, 1–9. https://doi.org/10.1371/journal.pone.0012444 (2010).Article 
    CAS 

    Google Scholar 
    IUCN – SSC Cetacean Specialist Group. Status of the World’s cetaceans (2021). https://iucn-csg.org/status-of-the-worlds-cetaceans/.Bailey, H. et al. Behavioural estimation of blue whale movements in the Northeast Pacific from state-space model analysis of satellite tracks. Endanger. Species Res. 10, 93–106. https://doi.org/10.3354/esr00239 (2010).Article 

    Google Scholar 
    Thomas, P. O., Reeves, R. R. & Brownell, R. L. Jr. Status of the world’s baleen whales. Mar. Mamm. Sci. 32, 682–734. https://doi.org/10.1111/mms.12281 (2016).Article 

    Google Scholar 
    Grigoli, F. et al. Current challenges in monitoring, discrimination, and management of induced seismicity related to underground industrial activities: A European perspective. Rev. Geophys. 55, 310–340. https://doi.org/10.1002/2016RG000542 (2017).Article 
    ADS 

    Google Scholar 
    Bigg, G. R. & Hanna, E. Impacts and effects of ocean warming on the weather. In: Laffoley, D. & Baxter, J. M. (eds.) Explaining ocean warming: Causes, scale, effects and consequences, 359–372, https://doi.org/10.2305/IUCN.CH.2016.08.en (International Union for Conservation of Nature and Natural Resources (IUCN), Gland, Switzerland, 2016).Hartog, A. H. An Introduction to Distributed Optical Fibre Sensors 1st edn. (CRC Press, 2017). https://doi.org/10.1201/9781315119014.Book 

    Google Scholar 
    Lin, J., Fang, S., Li, X., Wu, R. & Zheng, H. Seismological observations of ocean swells induced by Typhoon Megi using dispersive microseisms recorded in coastal areas. Remote Sens.https://doi.org/10.3390/rs10091437 (2018).Article 

    Google Scholar 
    Munk, W. H., Miller, G. R., Snodgrass, F. E., Barber, N. F. & Deacon, G. E. R. Directional recording of swell from distant storms. Philos. Trans. R. Soc. Lond. Ser. A Math. Phys. Sci. 255, 505–584. https://doi.org/10.1098/rsta.1963.0011 (1963).Article 
    ADS 

    Google Scholar 
    Mellinger, D. K. & Clark, C. W. Blue whale (balaenoptera musculus) sounds from the North Atlantic. J. Acoust. Soc. Am. 114, 1108–1119. https://doi.org/10.1121/1.1593066 (2003).Article 
    ADS 
    PubMed 

    Google Scholar 
    Ou, H., Au, W. W., Van Parijs, S., Oleson, E. M. & Rankin, S. Discrimination of frequency-modulated baleen whale downsweep calls with overlapping frequencies. J. Acoust. Soc. Am. 137, 3024–3032. https://doi.org/10.1121/1.4919304 (2015).Article 
    ADS 
    PubMed 

    Google Scholar 
    Saito, T. & Tsushima, H. Synthesizing ocean bottom pressure records including seismic wave and tsunami contributions: Toward realistic tests of monitoring systems. J. Geophys. Res. Solid Earth 121, 8175–8195. https://doi.org/10.1002/2016JB013195 (2016).Article 
    ADS 

    Google Scholar 
    Rørstadbotnen, R. A. et al. Analysis of a local earthquake in the Arctic using a 120 km long fibre-optic cable. In 83rd EAGE Annual Conference & Exhibition, vol. 2022 of Conference Proceedings, 1–5, https://doi.org/10.3997/2214-4609.202210404 (European Association of Geoscientists & Engineers, 2022).Bromirski, P. D. & Duennebier, F. K. The near-coastal microseism spectrum: Spatial and temporal wave climate relationships. J. Geophys. Res. Solid Earth 107, ESE 5-1-20. https://doi.org/10.1029/2001JB000265 (2002).Article 

    Google Scholar 
    Pasch, R. J. National hurricane center tropical cyclone report: Tropical storm Edouard (AL052020). Technical report, National Oceanic and Atmospheric Administration (2021). https://www.nhc.noaa.gov/data/tcr/AL052020_Edouard.pdf.Gobato, R. & Heidari, A. Cyclone Bomb hits Southern Brazil in 2020. J. Atmos. Sci. Res. 3, 8–12. https://doi.org/10.30564/jasr.v3i3.2163 (2020).Article 

    Google Scholar 
    Khalid, A., de Lima, Ad. S., Cassalho, F., Miesse, T. & Ferreira, C. Hydrodynamic and wave responses during storm surges on the Southern Brazilian Coast: A real-time forecast system. Water 12, 3397. https://doi.org/10.3390/w12123397 (2020).Article 

    Google Scholar 
    Ćirić, J. Weather warning for Central Highland, Northwest Iceland (2020). https://www.icelandreview.com/travel/weather-warning-for-central-highland-northwest-iceland/.Schoeman, R. P., Patterson-Abrolat, C. & Plön, S. A global review of vessel collisions with marine animals. Front. Mar. Sci. 7, 292. https://doi.org/10.3389/fmars.2020.00292 (2020).Article 

    Google Scholar 
    Ringrose, P. S. et al. Storage of carbon dioxide in saline aquifers: Physicochemical processes, key constraints, and scale-up potential. Annu. Rev. Chem. Biomol. Eng. 12, 471–494. https://doi.org/10.1146/annurev-chembioeng-093020-091447 (2021).Article 
    CAS 
    PubMed 

    Google Scholar 
    Nishimura, T. et al. Source location of volcanic earthquakes and subsurface characterization using fiber-optic cable and distributed acoustic sensing system. Sci. Rep. 11, 6319. https://doi.org/10.1038/s41598-021-85621-8 (2021).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ardhuin, F. & Herbers, T. H. C. Noise generation in the solid Earth, oceans and atmosphere, from nonlinear interacting surface gravity waves in finite depth. J. Fluid Mech. 716, 316–348. https://doi.org/10.1017/jfm.2012.548 (2013).Article 
    ADS 
    MATH 

    Google Scholar 
    Airy, G. B. Encyclopaedia Metropolitana (1817–1845), vol. 3 of Mixed Sciences, chap. Tides and waves (London, 1841).Craik, A. D. The origins of water wave theory. Annu. Rev. Fluid Mech. 36, 1–28. https://doi.org/10.1146/annurev.fluid.36.050802.122118 (2004).Article 
    ADS 
    MathSciNet 
    MATH 

    Google Scholar 
    Matsumoto, H., Inoue, S. & Ohmachi, T. Dynamic response of bottom water pressure due to the 2011 Tohoku earthquake. J. Disaster Res. 7, 468–475. https://doi.org/10.20965/jdr.2012.p0468 (2012).Article 

    Google Scholar 
    Landrø, M. & Hatchell, P. Normal modes in seismic data: Revisited. Geophysics 77, W27–W40. https://doi.org/10.1190/geo2011-0094.1 (2012).Article 
    ADS 

    Google Scholar  More

  • in

    Plant-frugivore network simplification under habitat fragmentation leaves a small core of interacting generalists

    Bascompte, J. & Jordano, P. Mutualistic Networks (Princeton Univ. Press, Princeton, NJ, 2013).Cordeiro, N. J. & Howe, H. F. Forest fragmentation severs mutualism between seed dispersers and an endemic African tree. Proc. Natl Acad. Sci. USA 100, 14052–14056 (2003).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wandrag, E. M., Dunham, A. E., Duncan, R. P. & Rogers, H. S. Seed dispersal increases local species richness and reduces spatial turnover of tropical tree seedlings. Proc. Natl Acad. Sci. USA 114, 10689–10694 (2017).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Fahrig, L. Effects of habitat fragmentation on biodiversity. Annu. Rev. Ecol. Evol. Syst. 34, 487–515 (2003).
    Google Scholar 
    Fahrig, L. Ecological responses to habitat fragmentation per se. Annu. Rev. Ecol. Evol. Syst. 48, 1–23 (2017).
    Google Scholar 
    Haddad, N. M. et al. Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci. Adv. 1, e1500052 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    Fricke, E. C. & Svenning, J. C. Accelerating homogenization of the global plant-frugivore meta-network. Nature 585, 74–78 (2020).CAS 
    PubMed 

    Google Scholar 
    Fontúrbel, F. E. et al. Meta-analysis of anthropogenic habitat disturbance effects on animal-mediated seed dispersal. Glob. Change Biol. 21, 3951–3960 (2015).
    Google Scholar 
    Poisot, T. et al. Global knowledge gaps in species interaction networks data. J. Biogeogr. 48, 1552–1563 (2021).
    Google Scholar 
    Hortal, J. et al. Seven shortfalls that beset large-scale knowledge of biodiversity. Annu. Rev. Ecol. Evol. Syst. 46, 523–549 (2015).
    Google Scholar 
    Magrach, A., Laurance, W. F., Larrinaga, A. R. & Santamaria, L. Meta-analysis of the effects of forest fragmentation on interspecific interactions. Conserv. Biol. 28, 1342–1348 (2014).PubMed 

    Google Scholar 
    Pocock, M. J. O., Evans, D. M. & Memmott, J. The robustness and restoration of a network of ecological networks. Science 335, 973–977 (2012).CAS 
    PubMed 

    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 

    Google Scholar 
    de Assis Bomfim, J., Guimarães, P. R. Jr., Peres, C. A., Carvalho, G. & Cazetta, E. Local extinctions of obligate frugivores and patch size reduction disrupt the structure of seed dispersal networks. Ecography 41, 1899–1909 (2018).
    Google Scholar 
    Emer, C. et al. Seed dispersal networks in tropical forest fragments: Area effects, remnant species, and interaction diversity. Biotropica 52, 81–89 (2020).
    Google Scholar 
    Evans, D. M., Pocock, M. J. O. & Memmott, J. The robustness of a network of ecological networks to habitat loss. Ecol. Lett. 16, 844–852 (2013).PubMed 

    Google Scholar 
    Grass, I., Jauker, B., Steffan-Dewenter, I., Tscharntke, T. & Jauker, F. Past and potential future effects of habitat fragmentation on structure and stability of plant-pollinator and host-parasitoid networks. Nat. Ecol. Evol. 2, 1408–1417 (2018).PubMed 

    Google Scholar 
    Neff, F. M. et al. Changes in plant-herbivore network structure and robustness along land-use intensity gradients in grasslands and forests. Sci. Adv. 7, eabf3985 (2021).PubMed 
    PubMed Central 

    Google Scholar 
    Dunne, J. A., Williams, R. J. & Martinez, N. D. Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecol. Lett. 5, 558–567 (2002).
    Google Scholar 
    James, A., Pitchford, J. W. & Plank, M. J. Disentangling nestedness from models of ecological complexity. Nature 487, 227–230 (2012).CAS 
    PubMed 

    Google Scholar 
    Jordano, P. Patterns of mutualistic interactions in pollination and seed dispersal: connectance, dependence asymmetries, and coevolution. Am. Nat. 129, 657–677 (1987).
    Google Scholar 
    Vieira, M. C. & Almeida-Neto, M. A simple stochastic model for complex coextinctions in mutualistic networks: robustness decreases with connectance. Ecol. Lett. 18, 144–152 (2015).PubMed 

    Google Scholar 
    Olesen, J. M., Bascompte, J., Dupont, Y. L. & Jordano, P. The modularity of pollination networks. Proc. Natl Acad. Sci. USA 104, 19891–19896 (2007).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gilarranz, L. J., Rayfield, B., Liñán-Cembrano, G., Bascompte, J. & Gonzalez, A. Effects of network modularity on the spread of perturbation impact in experimental metapopulations. Science 357, 199–201 (2017).CAS 
    PubMed 

    Google Scholar 
    Liu, H. et al. Geographic variation in the robustness of pollination networks is mediated by modularity. Glob. Ecol. Biogeogr. 30, 1447–1460 (2021).
    Google Scholar 
    Bascompte, J., Jordano, P., Melián, C. J. & Olesen, J. M. The nested assembly of plant-animal mutualistic networks. Proc. Natl Acad. Sci. USA 100, 9383–9387 (2003).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bastolla, U. et al. The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458, 1018–1020 (2009).CAS 
    PubMed 

    Google Scholar 
    Memmott, J., Waser, N. M. & Price, M. V. Tolerance of pollination networks to species extinctions. Proc. R. Soc. B. 271, 2605–2611 (2004).PubMed 
    PubMed Central 

    Google Scholar 
    Delmas, E. et al. Analysing ecological networks of species interactions. Biol. Rev. 9, 16–36 (2019).
    Google Scholar 
    Fortuna, M. A. et al. Nestedness versus modularity in ecological networks: two sides of the same coin? J. Anim. Ecol. 79, 811–817 (2010).PubMed 

    Google Scholar 
    Song, C., Rohr, R. P. & Saavedra, S. Why are some plant-pollinator networks more nested than others? J. Anim. Ecol. 86, 1417–1424 (2017).PubMed 

    Google Scholar 
    Schleuning, M., Böhning-Gaese, K., Dehling, D. M. & Burns, K. C. At a loss for birds: insularity increases asymmetry in seed-dispersal networks. Glob. Ecol. Biogeogr. 23, 385–394 (2014).
    Google Scholar 
    Aizen, M. A., Sabatino, M. & Tylianakis, J. M. Specialization and rarity predict nonrandom loss of interactions from mutualist networks. Science 335, 1486–1489 (2012).CAS 
    PubMed 

    Google Scholar 
    Fortuna, M. A. & Bascompte, J. Habitat loss and the structure of plant-animal mutualistic networks. Ecol. Lett. 9, 278–283 (2006).
    Google Scholar 
    Spiesman, B. J. & Inouye, B. D. Habitat loss alters the architecture of plant-pollinator interaction networks. Ecology 94, 2688–2696 (2013).PubMed 

    Google Scholar 
    Traveset, A. et al. Bird-flower visitation networks in the Galápagos unveil a widespread interaction release. Nat. Commun. 6, 6376 (2015).CAS 
    PubMed 

    Google Scholar 
    Thébault, E. & Fontaine, C. Stability of ecological communities and the architecture of mutualistic and trophic networks. Science 329, 853–856 (2010).PubMed 

    Google Scholar 
    Monteiro, E. C. S., Pizo, M. A., Vancine, M. H. & Ribeiro, M. C. Forest cover and connectivity have pervasive effects on the maintenance of evolutionary distinct interactions in seed dispersal networks. Oikos 2022, e08240 (2022).
    Google Scholar 
    Whittaker, R. J., Fernández-Palacios, J. M., Matthews, T. J., Borregaard, M. K. & Triantis, K. A. Island biogeography: taking the long view of nature’s laboratories. Science 357, eaam8326 (2017).PubMed 

    Google Scholar 
    Vizentin-Bugoni, J. et al. Structure, spatial dynamics, and stability of novel seed dispersal mutualistic networks in Hawai’i. Science 364, 78–82 (2019).CAS 
    PubMed 

    Google Scholar 
    Diamond, J. Dammed experiments! Science 294, 1847–1848 (2001).CAS 
    PubMed 

    Google Scholar 
    Jones, I. L., Bunnefeld, N., Jump, A. S., Peres, C. A. & Dent, D. H. Extinction debt on reservoir land-bridge islands. Biol. Conserv. 199, 75–83 (2016).
    Google Scholar 
    Wu, J., Huang, J., Han, X., Xie, Z. & Gao, X. Three-Gorges dam–experiment in habitat Fragmentation? Science 300, 1239–1240 (2003).CAS 
    PubMed 

    Google Scholar 
    Wilson, M. C. et al. Habitat fragmentation and biodiversity conservation: key findings and future challenges. Landsc. Ecol. 31, 219–227 (2016).
    Google Scholar 
    Trøjelsgaard, K. et al. Island biogeography of mutualistic interaction networks. J. Biogeogr. 40, 2020–2031 (2013).
    Google Scholar 
    Emer, C., Venticinque, E. M. & Fonseca, C. R. Effects of dam-induced landscape fragmentation on amazonian ant-plant mutualistic networks. Conserv. Biol. 27, 763–773 (2013).PubMed 

    Google Scholar 
    Zhu, C. et al. Arboreal camera trapping: a reliable tool to monitor plant-frugivore interactions in the trees on large scales. Remote Sens. Ecol. Conserv. 8, 92–104 (2022).
    Google Scholar 
    Zhu, C., Li, W., Wang, D., Ding, P. & Si, X. Plant-frugivore interactions revealed by arboreal camera trapping. Front. Ecol. Environ. 19, 149–151 (2021).
    Google Scholar 
    Galiana, N. et al. The spatial scaling of species interaction networks. Nat. Ecol. Evol. 2, 782–790 (2018).PubMed 

    Google Scholar 
    Hanski, I., Zurita, G. A., Bellocq, M. I. & Rybicki, J. Species-fragmented area relationship. Proc. Natl Acad. Sci. USA 110, 12715–12720 (2013).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sugiura, S. Species interactions-area relationships: biological invasions and network structure in relation to island area. Proc. R. Soc. B. 277, 1807–1815 (2010).PubMed 
    PubMed Central 

    Google Scholar 
    Galiana, N. et al. Ecological network complexity scales with area. Nat. Ecol. Evol. 6, 307–314 (2022).PubMed 

    Google Scholar 
    Santos, M., Cagnolo, L., Roslin, T., Marrero, H. J. & Vázquez, D. P. Landscape connectivity explains interaction network patterns at multiple scales. Ecology 100, e02883 (2019).PubMed 

    Google Scholar 
    Si, X., Pimm, S. L., Russell, G. J. & Ding, P. Turnover of breeding bird communities on islands in an inundated lake. J. Biogeogr. 41, 2283–2292 (2014).
    Google Scholar 
    Si, X. et al. Functional and phylogenetic structure of island bird communities. J. Anim. Ecol. 86, 532–542 (2017).PubMed 

    Google Scholar 
    Rosenfeld, J. S. Functional redundancy in ecology and conservation. Oikos 98, 156–162 (2002).
    Google Scholar 
    Sebastián-González, E. Drivers of species’ role in avian seed-dispersal mutualistic networks. J. Anim. Ecol. 86, 878–887 (2017).PubMed 

    Google Scholar 
    Donoso, I. et al. Downsizing of animal communities triggers stronger functional than structural decay in seed-dispersal networks. Nat. Commun. 11, 1582 (2020).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kaiser-Bunbury, C. N., Muff, S., Memmott, J., Müller, C. B. & Caflisch, A. The robustness of pollination networks to the loss of species and interactions: a quantitative approach incorporating pollinator behaviour. Ecol. Lett. 13, 442–452 (2010).PubMed 

    Google Scholar 
    Dalsgaard, B. et al. Opposed latitudinal patterns of network-derived and dietary specialization in avian plant-frugivore interaction systems. Ecography 40, 1395–1401 (2017).
    Google Scholar 
    Borrvall, C., Ebenman, B. & Jonsson, T. Biodiversity lessens the risk of cascading extinction in model food webs. Ecol. Lett. 3, 131–136 (2000).
    Google Scholar 
    Liao, J. et al. Robustness of metacommunities with omnivory to habitat destruction: disentangling patch fragmentation from patch loss. Ecology 98, 1631–1639 (2017).PubMed 

    Google Scholar 
    Rumeu, B. et al. Predicting the consequences of disperser extinction: richness matters the most when abundance is low. Funct. Ecol. 31, 1910–1920 (2017).
    Google Scholar 
    Wong, B. B. M. & Candolin, U. Behavioral responses to changing environments. Behav. Ecol. 26, 665–673 (2015).
    Google Scholar 
    Betts, M. G. et al. Extinction filters mediate the global effects of habitat fragmentation on animals. Science 366, 1236–1239 (2019).CAS 
    PubMed 

    Google Scholar 
    Menke, S., Böhning-Gaese, K. & Schleuning, M. Plant-frugivore networks are less specialized and more robust at forest–farmland edges than in the interior of a tropical forest. Oikos 121, 1553–1566 (2012).
    Google Scholar 
    Redhead, J. W. et al. Potential landscape-scale pollinator networks across Great Britain: structure, stability and influence of agricultural land cover. Ecol. Lett. 21, 1821–1832 (2018).PubMed 

    Google Scholar 
    Si, X. et al. The importance of accounting for imperfect detection when estimating functional and phylogenetic community structure. Ecology 99, 2103–2112 (2018).PubMed 

    Google Scholar 
    Schoereder, J. H. et al. Should we use proportional sampling for species-area studies? J. Biogeogr. 31, 1219–1226 (2004).
    Google Scholar 
    Liu, J. et al. The distribution of plants and seed dispersers in response to habitat fragmentation in an artificial island archipelago. J. Biogeogr. 46, 1152–1162 (2019).
    Google Scholar 
    Olson, E. R. et al. Arboreal camera trapping for the Critically Endangered greater bamboo lemur Prolemur simus. Oryx 46, 593–597 (2012).
    Google Scholar 
    Li, H.-D. et al. The functional roles of species in metacommunities, as revealed by metanetwork analyses of bird-plant frugivory networks. Ecol. Lett. 23, 1252–1262 (2020).PubMed 

    Google Scholar 
    Snow, B. & Snow, D. Birds and berries: a study of an ecological interaction (T & AD Poyser, Calton, 1988).Si, X., Kays, R. & Ding, P. How long is enough to detect terrestrial animals? Estimating the minimum trapping effort on camera traps. PeerJ 2, e374 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    Vázquez, D. P. et al. Species abundance and asymmetric interaction strength in ecological networks. Oikos 116, 1120–1127 (2007).
    Google Scholar 
    Chao, A. & Jost, L. Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93, 2533–2547 (2012).PubMed 

    Google Scholar 
    Hsieh, T. C., Ma, K. H. & Chao, A. iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol. Evol. 7, 1451–1456 (2016).
    Google Scholar 
    Beckett, S. J. Improved community detection in weighted bipartite networks. R. Soc. Open. Sci. 3, 140536 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Almeida-Neto, M. & Ulrich, W. A straightforward computational approach for measuring nestedness using quantitative matrices. Environ. Modell. Softw. 26, 173–178 (2011).
    Google Scholar 
    Scherber, C. et al. Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment. Nature 468, 553–556 (2010).CAS 
    PubMed 

    Google Scholar 
    Schleuning, M. et al. Ecological networks are more sensitive to plant than to animal extinction under climate change. Nat. Commun. 7, 13965 (2016).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Humphreys, A. M., Govaerts, R., Ficinski, S. Z., Nic Lughadha, E. & Vorontsova, M. S. Global dataset shows geography and life form predict modern plant extinction and rediscovery. Nat. Ecol. Evol. 3, 1043–1047 (2019).PubMed 

    Google Scholar 
    Dirzo, R. et al. Defaunation in the Anthropocene. Science 345, 401–406 (2014).CAS 
    PubMed 

    Google Scholar 
    Rogers, H. S., Donoso, I., Traveset, A. & Fricke, E. C. Cascading impacts of seed disperser loss on plant communities and ecosystems. Annu. Rev. Ecol. Evol. Syst. 52, 641–666 (2021).
    Google Scholar 
    Dormann, C. F., Gruber, B. & Fründ, J. Introducing the bipartite package: analysing ecological networks. R News 8, 8–11 (2008).
    Google Scholar 
    Patefield, W. M. Algorithm AS 159: An efficient method of generating random R × C tables with given row and column totals. Appl. Stat. 30, 91–97 (1981).
    Google Scholar 
    Lefcheck, J. S. piecewiseSEM: piecewise structural equation modelling in R for ecology, evolution, and systematics. Methods Ecol. Evol. 7, 573–579 (2016).
    Google Scholar 
    Kabacoff, R. R in Action: Data Analysis and Graphics with R (Manning Publications Co, 2015).R Core Team. R: A Language And Environment For Statistical Computing (R Foundation for Statistical Computing, 2021). More

  • in

    Plant-associated Bacillus mobilizes its secondary metabolites upon perception of the siderophore pyochelin produced by a Pseudomonas competitor

    Nayfach S, Roux S, Seshadri R, Udwary D, Varghese N, Schulz F, et al. A genomic catalog of Earth’s microbiomes. Nat Biotechnol. 2021;39:499–509.CAS 
    PubMed 

    Google Scholar 
    Fierer N. Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Rev Microbiol. 2017;15:579–90.CAS 
    PubMed 

    Google Scholar 
    Cordovez V, Dini-Andreote F, Carrión VJ, Raaijmakers JM. Ecology and evolution of plant microbiomes. Annu Rev Microbiol. 2019;73:69–88.CAS 
    PubMed 

    Google Scholar 
    Trivedi P, Leach JE, Tringe SG, Sa T, Singh BK. Plant–microbiome interactions: from community assembly to plant health. Nat Rev Microbiol. 2020;18:607–21.CAS 
    PubMed 

    Google Scholar 
    Fitzpatrick CR, Salas-González I, Conway JM, Finkel OM, Gilbert S, Russ D, et al. The plant microbiome: From ecology to reductionism and beyond. Annu Rev Microbiol. 2020;74:81–100.CAS 
    PubMed 

    Google Scholar 
    Schmidt R, Ulanova D, Wick LY, Bode HB, Garbeva P. Microbe-driven chemical ecology: past, present and future. ISME J. 2019;13:2656–63.PubMed 
    PubMed Central 

    Google Scholar 
    Tyc O, Song C, Dickschat JS, Vos M, Garbeva P. The ecological role of volatile and soluble secondary metabolites produced by soil bacteria. Trends Microbiol. 2017;25:280–92.CAS 
    PubMed 

    Google Scholar 
    Romero D, Traxler MF, López D, Kolter R. Antibiotics as signal molecules. Chem Rev. 2011;111:5492–505.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Traxler MF, Seyedsayamdost MR, Clardy J, Kolter R. Interspecies modulation of bacterial development through iron competition and siderophore piracy. Mol Microbiol. 2012;86:628–44.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bernal P, Llamas MA, Filloux A. Type VI secretion systems in plant-associated bacteria. Environ Microbiol. 2018;20:1–15.PubMed 

    Google Scholar 
    Okada BK, Seyedsayamdost MR. Antibiotic dialogues: induction of silent biosynthetic gene clusters by exogenous small molecules. FEMS Microbiol Rev. 2017;41:19–33.CAS 
    PubMed 

    Google Scholar 
    Zhang C, Straight PD. Antibiotic discovery through microbial interactions. Curr Opin Microbiol. 2019;51:64–71.CAS 
    PubMed 

    Google Scholar 
    Traxler MF, Kolter R. Natural products in soil microbe interactions and evolution. Nat Prod Rep. 2015;32:956–70.CAS 
    PubMed 

    Google Scholar 
    Müller DB, Vogel C, Bai Y, Vorholt JA. The plant microbiota: systems-level insights and perspectives. Annu Rev Genet. 2016;50:211–34.PubMed 

    Google Scholar 
    Anckaert A, Arias AA, Hoff G, Calonne-Salmon M, Declerck S, Ongena M. The use of Bacillus spp. as bacterial biocontrol agents to control plant diseases. In: Köhl J, Ravensberg W, editors. Microbial bioprotectants for plant disease management. Cambridge, UK: Burleigh Dodds Science Publishing; 2022. p. 1–54.Dunlap CA. Taxonomy of registered Bacillus spp. strains used as plant pathogen antagonists. Biol Control. 2019;134:82–86.
    Google Scholar 
    Ye M, Tang X, Yang R, Zhang H, Li F, Tao F, et al. Characteristics and application of a novel species of Bacillus: Bacillus velezensis. ACS Chem Biol. 2018;13:500–5.CAS 
    PubMed 

    Google Scholar 
    Grubbs KJ, Bleich RM, Santa Maria KC, Allen SE, Farag S, Shank EA, et al. Large-scale bioinformatics analysis of Bacillus genomes uncovers conserved roles of natural products in bacterial physiology. mSystems 2017;2:e00040–17.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Harwood CR, Mouillon J-MM, Pohl S, Arnau J. Secondary metabolite production and the safety of industrially important members of the Bacillus subtilis group. FEMS Microbiol Rev. 2018;42:721–38.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Köhl J, Kolnaar R, Ravensberg WJ. Mode of action of microbial biological control agents against plant diseases: Relevance beyond efficacy. Front Plant Sci. 2019;10:1–19.
    Google Scholar 
    Li Y, Rebuffat S. The manifold roles of microbial ribosomal peptide-based natural products in physiology and ecology. J Biol Chem. 2020;295:34–54.Andrić S, Meyer T, Ongena M. Bacillus responses to plant-associated fungal and bacterial communities. Front Microbiol. 2020;11:1350.PubMed 
    PubMed Central 

    Google Scholar 
    Zhang L, Sun C. Fengycins, cyclic lipopeptides from marine Bacillus subtilis strains, kill the plant-pathogenic fungus Magnaporthe grisea by inducing reactive oxygen species production and chromatin condensation. Appl Environ Microbiol. 2018;84:e00445–18.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Molina-Santiago C, Vela-Corcía D, Petras D, Díaz-Martínez L, Pérez-Lorente AI, Sopeña-Torres S, et al. Chemical interplay and complementary adaptative strategies toggle bacterial antagonism and co-existence. Cell Rep. 2021;36:109449.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Molina-Santiago C, Pearson JR, Navarro Y, Berlanga-Clavero MV, Caraballo-Rodriguez AM, Petras D, et al. The extracellular matrix protects Bacillus subtilis colonies from Pseudomonas invasion and modulates plant co-colonization. Nat Commun. 2019;10:1919.PubMed 
    PubMed Central 

    Google Scholar 
    Almoneafy AA, Kakar KU, Nawaz Z, Li B, Saand MA, Chun-lan Y, et al. Tomato plant growth promotion and antibacterial related-mechanisms of four rhizobacterial Bacillus strains against Ralstonia solanacearum. Symbiosis 2014;63:59–70.CAS 

    Google Scholar 
    Kakar KU, Duan Y-P, Nawaz Z, Sun G, Almoneafy AA, Hassan MA, et al. A novel rhizobacterium Bk7 for biological control of brown sheath rot of rice caused by Pseudomonas fuscovaginae and its mode of action. Eur J Plant Pathol. 2014;138:819–34.
    Google Scholar 
    Raynaud X, Nunan N. Spatial ecology of bacteria at the microscale in soil. PLoS ONE. 2014;9:e87217.PubMed 
    PubMed Central 

    Google Scholar 
    Girard L, Lood C, Höfte M, Vandamme P, Rokni-Zadeh H, van Noort V, et al. The ever-expanding Pseudomonas genus: description of 43 new species and partition of the Pseudomonas putida group. Microorganisms. 2021;9:1–24.
    Google Scholar 
    Hua GKH, Höfte M. The involvement of phenazines and cyclic lipopeptide sessilin in biocontrol of Rhizoctonia root rot on bean (Phaseolus vulgaris) by Pseudomonas sp. CMR12a is influenced by substrate composition. Plant Soil. 2015;388:243–53.CAS 

    Google Scholar 
    Ma Z, Hoang Hua GKH, Ongena M, Höfte M. Role of phenazines and cyclic lipopeptides produced by Pseudomonas sp. CMR12a in induced systemic resistance on rice and bean. Environ Microbiol Rep. 2016;8:896–904.PubMed 

    Google Scholar 
    Olorunleke FE, Hua GKH, Kieu NP, Ma Z, Höfte M. Interplay between orfamides, sessilins and phenazines in the control of Rhizoctonia diseases by Pseudomonas sp. CMR12a. Environ Microbiol Rep. 2015;7:774–81.CAS 
    PubMed 

    Google Scholar 
    van Gestel J, Vlamakis H, Kolter R. From cell differentiation to cell collectives: Bacillus subtilis uses division of labor to migrate. PLoS Biol. 2015;13:1–29.
    Google Scholar 
    Nihorimbere V, Cawoy H, Seyer A, Brunelle A, Thonart P, Ongena M. Impact of rhizosphere factors on cyclic lipopeptide signature from the plant beneficial strain Bacillus amyloliquefaciens S499. FEMS Microbiol Ecol. 2012;79:176–91.CAS 
    PubMed 

    Google Scholar 
    Hoff G, Arias AA, Boubsi F, Pršić J, Meyer T, Ibrahim HMM, et al. Surfactin stimulated by pectin molecular patterns and root exudates acts as a key driver of the Bacillus-plant mutualistic interaction. MBio 2021;12:e01774–21.CAS 
    PubMed Central 

    Google Scholar 
    Andrić S, Meyer T, Rigolet A, Prigent-Combaret C, Höfte M, Balleux G, et al. Lipopeptide interplay mediates molecular interactions between soil bacilli and pseudomonads. Microbiol Spectr. 2021;9:e0203821.PubMed 

    Google Scholar 
    Pluskal T, Castillo S, Villar-Briones A, Orešič M. MZmine 2: modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data. BMC Bioinform. 2010;11:395.
    Google Scholar 
    Li W, Godzik A. Cd-hit: A fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics. 2006;22:1658–9.CAS 
    PubMed 

    Google Scholar 
    Bodenhofer U, Bonatesta E, Horejš-Kainrath C, Hochreiter S. msa: an R package for multiple sequence alignment. Bioinformatics. 2015;31:3997–9.CAS 
    PubMed 

    Google Scholar 
    Paradis E, Claude J, Strimmer K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 2004;20:289–90.CAS 
    PubMed 

    Google Scholar 
    Ivica Letunic PB. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 2021;49:W293–W296.PubMed 
    PubMed Central 

    Google Scholar 
    R Core Team (2020). R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2020.Steinke K, Mohite OS, Weber T, Kovács ÁT. Phylogenetic distribution of secondary metabolites in the Bacillus subtilis species complex. mSystems. 2021;6:2–10.
    Google Scholar 
    Molinatto G, Puopolo G, Sonego P, Moretto M, Engelen K, Viti C, et al. Complete genome sequence of Bacillus amyloliquefaciens subsp. plantarum S499, a rhizobacterium that triggers plant defences and inhibits fungal phytopathogens. J Biotechnol. 2016;238:56–59.CAS 
    PubMed 

    Google Scholar 
    Fan B, Wang C, Song X, Ding X, Wu L, Wu H, et al. Bacillus velezensis FZB42 in 2018: The gram-positive model strain for plant growth promotion and biocontrol. Front Microbiol. 2018;9:3389.
    Google Scholar 
    Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M, Ronald P, et al. Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol. 2012;13:614–29.PubMed 
    PubMed Central 

    Google Scholar 
    Scholz R, Vater J, Budiharjo A, Wang Z, He Y, Dietel K, et al. Amylocyclicin, a novel circular bacteriocin produced by Bacillus amyloliquefaciens FZB42. J Bacteriol. 2014;196:1842–52.PubMed 
    PubMed Central 

    Google Scholar 
    Lembrechts JJ, van den Hoogen J, Aalto J, Ashcroft MB, De Frenne P, Kemppinen J, et al. Global maps of soil temperature. Glob Chang Biol. 2022;28:3110–44.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Blake C, Christensen MN, Kovacs AT. Molecular aspects of plant growth promotion and protection by Bacillus subtilis. Mol Plant-Microbe Interact. 2021;34:15–25.CAS 
    PubMed 

    Google Scholar 
    Arnaouteli S, Bamford NC, Stanley-Wall NR, Kovács ÁT. Bacillus subtilis biofilm formation and social interactions. Nat Rev Microbiol. 2021;19:600–14.CAS 
    PubMed 

    Google Scholar 
    D’aes J, Hua GKH, De Maeyer K, Pannecoucque J, Forrez I, Ongena M, et al. Biological control of Rhizoctonia root rot on bean by phenazine- and cyclic lipopeptide-producing Pseudomonas CMR12a. Phytopathology. 2011;101:996–1004.PubMed 

    Google Scholar 
    Grandchamp GM, Caro L, Shank EA. Pirated siderophores promote sporulation in Bacillus subtilis. Appl Environ Microbiol. 2017;83:e03293–16.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Miethke M, Klotz O, Linne U, May JJ, Beckering CL, Marahiel MA. Ferri-bacillibactin uptake and hydrolysis in Bacillus subtilis. Mol Microbiol. 2006;61:1413–27.CAS 
    PubMed 

    Google Scholar 
    Pi H, Helmann JD. Genome-wide characterization of the fur regulatory network reveals a link between catechol degradation and bacillibactin metabolism in Bacillus subtilis. MBio. 2018;9:1–15.
    Google Scholar 
    Adler C, Corbalán NS, Seyedsayamdost MR, Pomares MF, de Cristóbal RE, Clardy J, et al. Catecholate siderophores protect bacteria from pyochelin toxicity. PLoS ONE. 2012;7:e46754.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Trottmann F, Franke J, Ishida K, García-Altares M, Hertweck C. A pair of bacterial siderophores releases and traps an intercellular signal molecule: an unusual case of natural nitrone bioconjugation. Angew Chem. 2019;58:200–4.CAS 

    Google Scholar 
    Mongkolsuk S, Helmann JD. Regulation of inducible peroxide stress responses. Mol Microbiol. 2002;45:9–15.CAS 
    PubMed 

    Google Scholar 
    Cox CD, Rinehart KL, Moore ML, Cook JC. Pyochelin: novel structure of an iron-chelating growth promoter for Pseudomonas aeruginosa. Proc Natl Acad Sci USA. 1981;78:4256–60.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Youard ZA, Mislin GLA, Majcherczyk PA, Schalk IJ, Reimmann C. Pseudomonas fluorescens CHA0 produces enantio-pyochelin, the optical antipode of the Pseudomonas aeruginosa siderophore pyochelin. J Biol Chem. 2007;282:35546–53.CAS 
    PubMed 

    Google Scholar 
    Ronnebaum TA, Lamb AL. Nonribosomal peptides for iron acquisition: pyochelin biosynthesis as a case study. Curr Opini Struct Biol. 2018;53:1–11.CAS 

    Google Scholar 
    Seipke RF, Song L, Bicz J, Laskaris P, Yaxley AM, Challis GL, et al. The plant pathogen Streptomyces scabies 87-22 has a functional pyochelin biosynthetic pathway that is regulated by TetR- and AfsR-family proteins. Microbiology. 2011;157:2681–93.CAS 
    PubMed 

    Google Scholar 
    Gu S, Wei Z, Shao Z, Friman VP, Cao K, Yang T, et al. Competition for iron drives phytopathogen control by natural rhizosphere microbiomes. Nat Microbiol. 2020;5:1002–10.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Komaki H, Ichikawa N, Hosoyama A, Hamada M, Igarashi Y. In silico analysis of PKS and NRPS gene clusters in arisostatin-and kosinostatin-producers and description of Micromonospora okii sp. nov. Antibiotics. 2021;10:1447.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Engelbrecht A, Saad H, Gross H, Kaysser L. Natural products from Nocardia and their role in pathogenicity. Micro Physiol. 2021;31:217–32.
    Google Scholar 
    Inahashi Y, Zhou S, Bibb MJ, Song L, Al-Bassam MM, Bibb MJ, et al. Watasemycin biosynthesis in Streptomyces venezuelae: thiazoline C-methylation by a type B radical-SAM methylase homologue. Chem Sci. 2017;8:2823–31.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Song J, Qiu S, Zhao J, Han C, Wang Y, Sun X, et al. Pseudonocardia tritici sp. nov., a novel actinomycete isolated from rhizosphere soil of wheat (Triticum aestivum L.). Nat Microbiol. 2019;12:470–80.
    Google Scholar 
    Sayed AM, Abdel-Wahab NM, Hassan HM, Abdelmohsen UR. Saccharopolyspora: an underexplored source for bioactive natural products. J Appl Microbiol. 2020;128:314–29.CAS 
    PubMed 

    Google Scholar 
    Nordstedt NP, Jones ML. Genomic analysis of Serratia plymuthica MBSA-MJ1: A plant growth promoting rhizobacteria that improves water stress tolerance in greenhouse ornamentals. Front Microbiol. 2021;12:653556.PubMed 
    PubMed Central 

    Google Scholar 
    Zhalnina K, Louie KB, Hao Z, Mansoori N, Da Rocha UN, Shi S, et al. Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat Microbiol. 2018;3:470–80.CAS 
    PubMed 

    Google Scholar 
    Takahashi Y, Malisorn K, Kanchanasin P, Phongsopitanun W, Tanasupawat S, Spain AM, et al. Actinomadura rhizosphaerae sp. nov., isolated from rhizosphere soil of the plant Azadirachta indica. ISME J 2018;68:3012–6.
    Google Scholar 
    Takahashi Y. Genus Kitasatospora, taxonomic features and diversity of secondary metabolites. J Antibiot. 2017;70:506–13.CAS 

    Google Scholar 
    Bennur T, Kumar AR, Zinjarde S, Javdekar V. Nocardiopsis species: Incidence, ecological roles and adaptations. Microbiol Res. 2015;174:33–47.PubMed 

    Google Scholar 
    Walterson AM, Stavrinides J. Pantoea: Insights into a highly versatile and diverse genus within the Enterobacteriaceae. J Basic Microbiol. 2015;39:33–47.
    Google Scholar 
    Sungthong R, Nakaew N. The genus Nonomuraea: a review of a rare actinomycete taxon for novel metabolites. J Basic Microbiol. 2015;55:554–65.PubMed 

    Google Scholar 
    Müller S, Strack SN, Ryan SE, Kearns DB, Kirby JR. Predation by Myxococcus xanthus induces Bacillus subtilis to form spore-filled megastructures. Appl Environ Microbiol. 2015;81:203–10.PubMed 

    Google Scholar 
    Straight PD, Fischbach MA, Walsh CT, Rudner DZ, Kolter R. A singular enzymatic megacomplex from Bacillus subtilis. Proc Natl Acad Sci USA. 2007;104:305–10.CAS 
    PubMed 

    Google Scholar 
    Barger SR, Hoefler BC, Cubillos-Ruiz A, Russell WK, Russell DH, Straight PD. Imaging secondary metabolism of Streptomyces sp. Mg1 during cellular lysis and colony degradation of competing Bacillus subtilis. Antonie van Leeuwenhoek. 2012;102:435–45.CAS 
    PubMed 

    Google Scholar 
    Ogran A, Yardeni EH, Keren-Paz A, Bucher T, Jain R, Gilhar O, et al. The plant host induces antibiotic production to select the most-beneficial colonizers. Appl Environ Microbiol. 2019;85:1–15.
    Google Scholar 
    Rosenberg G, Steinberg N, Oppenheimer-Shaanan Y, Olender T, Doron S, Ben-Ari J, et al. Not so simple, not so subtle: The interspecies competition between Bacillus simplex and Bacillus subtilis and its impact on the evolution of biofilms. npj Biofilms Microbiomes. 2016;2:15027.PubMed 
    PubMed Central 

    Google Scholar 
    Straight PD, Willey JM, Kolter R. Interactions between Streptomyces coelicolor and Bacillus subtilis: Role of surfactants in raising aerial structures. J Bacteriol. 2006;188:4918–25.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Hoefler BC, Gorzelnik KV, Yang JY, Hendricks N, Dorrestein PC, Straight PD. Enzymatic resistance to the lipopeptide surfactin as identified through imaging mass spectrometry of bacterial competition. Proc Natl Acad Sci USA. 2012;109:13082–7.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Liu Y, Kyle S, Straight PD. Antibiotic stimulation of a Bacillus subtilis migratory response. mSphere 2018;3:e00586–17.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Qi G, Zhu F, Du P, Yang X, Qiu D, Yu Z, et al. Lipopeptide induces apoptosis in fungal cells by a mitochondria-dependent pathway. Peptides. 2010;31:1978–86.CAS 
    PubMed 

    Google Scholar 
    McCully LM, Bitzer AS, Seaton SC, Smith LM, Silby MW. Interspecies social spreading: interaction between two sessile soil bacteria leads to emergence of surface motility. mSphere. 2019;4:e00696–18.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Flemming HC, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S. Biofilms: an emergent form of bacterial life. Nat Rev Microbiol. 2016;14:563–75.CAS 
    PubMed 

    Google Scholar 
    Townsley L, Shank EA. Natural-product antibiotics: cues for modulating bacterial biofilm formation. Trends Microbiol. 2017;25:1016–26.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sun X, Xu Z, Xie J, Hesselberg-Thomsen V, Tan T, Zheng D, et al. Bacillus velezensis stimulates resident rhizosphere Pseudomonas stutzeri for plant health through metabolic interactions. ISME J. 2022;16:774–87.CAS 
    PubMed 

    Google Scholar 
    Dumas Z, Ross-Gillespie A, Kümmerli R. Switching between apparently redundant iron-uptake mechanisms benefits bacteria in changeable environments. Proc R Soc B Biol Sci. 2013;280:20131055.
    Google Scholar 
    Lee N, Kim W, Chung J, Lee Y, Cho S, Jang KS, et al. Iron competition triggers antibiotic biosynthesis in Streptomyces coelicolor during coculture with Myxococcus xanthus. ISME J. 2020;14:1111–24.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kramer J, Özkaya Ö, Kümmerli R. Bacterial siderophores in community and host interactions. Nat Rev Microbiol. 2020;18:152–63.CAS 
    PubMed 

    Google Scholar 
    Niehus R, Picot A, Oliveira NM, Mitri S, Foster KR. The evolution of siderophore production as a competitive trait. Evolution. 2017;71:1443–55.CAS 
    PubMed 

    Google Scholar 
    Ho YN, Lee HJ, Hsieh CT, Peng CC, Yang YL. Chemistry and biology of salicyl-capped siderophores. Stud Nat Prod Chem. 2018;59:431–90.Schalk IJ, Rigouin C, Godet J. An overview of siderophore biosynthesis among fluorescent Pseudomonads and new insights into their complex cellular organization. Environ Microbiol. 2020;22:1447–66.PubMed 

    Google Scholar 
    Deveau A, Gross H, Palin B, Mehnaz S, Schnepf M, Leblond P, et al. Role of secondary metabolites in the interaction between Pseudomonas fluorescens and soil microorganisms under iron-limited conditions. FEMS Microbiol Ecol. 2016;92:1–11.
    Google Scholar 
    Jenul C, Keim K, Jens J, Zeiler MJ, Schilcher K, Schurr M, et al. Pyochelin biotransformation shapes bacterial competition. bioRxiv. 2022. https://doi.org/10.1101/2022.04.18.486787.Ho YN, Hoo SY, Wang BW, Hsieh CT, Lin CC, Sun CH, et al. Specific inactivation of an antifungal bacterial siderophore by a fungal plant pathogen. ISME J. 2021;15:1858–61.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lopez-Medina E, Fan D, Coughlin LA, Ho EX, Lamont IL, Reimmann C, et al. Candida albicans inhibits Pseudomonas aeruginosa virulence through suppression of pyochelin and pyoverdine biosynthesis. PLoS Pathog. 2015;11:1–34.
    Google Scholar 
    Meisel JD, Panda O, Mahanti P, Schroeder FC, Kim DH. Chemosensation of bacterial secondary metabolites modulates neuroendocrine signaling and behavior of C. elegans. Cell. 2014;159:267–80.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Finkel OM, Castrillo G, Herrera Paredes S, Salas González I, Dangl JL. Understanding and exploiting plant beneficial microbes. Curr Opin Plant Biol. 2017;38:155–63.PubMed 
    PubMed Central 

    Google Scholar 
    Saad MM, Eida AA, Hirt H, Doerner P. Tailoring plant-associated microbial inoculants in agriculture: a roadmap for successful application. J Exp Bot. 2020;71:3878–901.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ansari FA, Ahmad I. Fluorescent Pseudomonas -FAP2 and Bacillus licheniformis interact positively in biofilm mode enhancing plant growth and photosynthetic attributes. Sci Rep. 2019;9:4547.PubMed 
    PubMed Central 

    Google Scholar 
    Domenech J, Reddy MS, Kloepper JW, Ramos B, Gutierrez-Mañero J. Combined application of the biological product LS213 with Bacillus, Pseudomonas or Chryseobacterium for growth promotion and biological control of soil-borne diseases in pepper and tomato. BioControl. 2006;51:245–58.CAS 

    Google Scholar 
    Powers MJ, Sanabria-Valentín E, Bowers AA, Shank EA. Inhibition of cell differentiation in Bacillus subtilis by Pseudomonas protegens. J Bacteriol. 2015;197:2129–38.CAS 
    PubMed 
    PubMed Central 

    Google Scholar  More

  • in

    Living on the sea-coast: ranging and habitat distribution of Asiatic lions

    Study areaSituated in western India’s southwestern part of the Gujarat state, the Saurashtra region typically represents the semi-arid Gujarat-Rajputana province 4B23, which covers 11 out of 33 districts of the state. The region forms a rocky tableland (altitude 300–600 m) fringed by coastal plains with an undulating central plain broken by hills and dissected by various rivers that flow in all directions24. With the longest coastline (~ 1600 km) in India, Gujarat is endowed with rich coastal biodiversity25,26. The Saurashtra coast in Gujarat is encircled by the open sea between two Gulfs (68° 58′–71° 30′ N and 22° 15′–20° 50′ E) and divided into two segments, viz. the southwestern coast from Dwarka to Diu (~ 300 km stretch) and south-eastern coast from Diu to Bhavnagar (~ 250 km stretch)26.The Asiatic Lion Landscape covers an area of ~ 30,000 km2 (permanent lion distribution range: ~ 16,000 km2; visitation record range: ~ 14,000 km2) of varied habitat types within Saurashtra. The landscape includes five protected areas (Gir National Park, Gir Wildlife Sanctuary, Paniya Wildlife Sanctuary, Mitiyala Wildlife Sanctuary, and Girnar Wildlife Sanctuary) and other forest classes (reserved forests, protected forests, and unclassed forests).The coastal habitats extend across the districts of Bhavnagar, Amreli, Gir-Somnath, and Junagadh (Fig. 1). Within these districts (Fig. 1), the tehsils (sub-divisions/taluka) of Mangrol, Malia, Patan-Veraval, Sutrapada, Kodinar and Una are categorized under the southwestern coast (hereafter western coastal habitat), Jafrabad, Rajula, form the south-eastern coast and Mahuva and Talaja constitute the Bhavnagar coast and represent distinct lion range units (Fig. 1). The total area covered in the study is 2843 km2 on the eastern coast and 1413 km2 on the western coast (Fig. 1).The Saurashtra region is bestowed with three distinct seasons, viz. dry and hot summer (March–June), monsoon (July–October), and primarily dry winter (November–February). It receives a mean annual rainfall of ~ 600 mm, with most rainfall during the southwest monsoon27. The mean maximum and minimum temperatures are 34 °C and 19 °C, respectively28. There is a 110 km2 stretch of forests along the coast. The rest of the areas are multi-use consisting of private, industrial, pastoral and wastelands of varied ownerships. The natural vegetation primarily consists of Prosopis juliflora and Casuarina equistsetifolia. On the beach and dune areas, vegetation such as Ipomea pescaprae, Sporobolus trinules, Fimrystylis sp., Crotalaria sp., and Euphorbia nivuleria29. The mudflats along the coast are restricted to Talaja, Mahuva, Pipavav Port, Jafrabad creek, and Porbandar, sparsely covered by the Avicennia marina29. Fisheries, agriculture, horticulture, livestock rearing, and some large- and small-scale industries are the leading economies in the coastal belt.Coastal segments are characterized by the variety of vegetation, sandy beaches, small cliffs, wave-cut platforms, open and submerged dunes, minor estuaries, embankments, and transition from the open sea to gulf environment with tidal mud26,29 and also support a diverse assemblage of biodiversity25. This biodiversity is further enriched by several perennial/ephemeral rivers originating from the Gir PA (Shetrunji, Machundari, Raval, Ardak, Bhuvatirth, Shinghoda, Hiran, Saraswati, etc.)12. These rivers meet the sea at different sections of the coast, forming prominent coastal ecosystems25. The riverine tracts act as important corridors for wildlife movement9,12,30. Dispersing through these corridors, lions have started inhabiting these coastal habitats30,31.MethodsAll the research activities involved in this study on Asiatic lions were carried out after taking due permission from the Ministry of Environment, Forests & Climate Change (MoEF&CC), Government of India (Letter No.: F. No. 1-50/2018 WL) and Principal Chief Conservator of Forests (Wildlife) & Chief Wildlife Warden, Gujarat State, Gandhinagar (Letter No.: WLP 26B 781-83/2019-20). Procedures and protocols were followed as per the Standard Operating Procedures of the Gujarat Forest Department, Government of Gujarat, concerning the handling of wild animals. Qualified and experienced veterinarians and their team carried out all procedures related to radio-collaring. Moreover, the study is reported in accordance with ‘Animal Research: Reporting of In Vivo Experiments’ (ARRIVE) guidelines as applicable.A long-term lion monitoring project was initiated in 2019 by the Gujarat Forest Department to understand the movement patterns and ecology of lions in the Asiatic Lion Landscape. Looking at the heterogeneity and vastness of the coastal areas, ten individuals were carefully selected for satellite radio-collaring based on their frequent movement in different coastal habitats and monitored from 2019 to 2021.The lions were deployed with Vertex Plus GPS Collars (Vectronics Aerospace GmbH, Berlin, Germany) that weighed less than three per cent of the individual’s body weight, irrespective of age and sex. The lions were immobilized using a combination of Ketamine hydrochloride (2.2 mg per kg body weight; Ketamine, Biowet, Pulawy) and Xylazine hydrochloride (1.1 mg per kg body weight; Xylaxil, Brilliant Bio Pharma Pvt. Ltd., Telangana)32 administered intramuscularly using a gas-powered Telinject™ G.U.T 50 (Telinject Inc., Dudenhofen, Germany) dart delivery system. A blindfold was placed to protect the eyes and decrease visual stimuli33,34. Each sedated individual was sexed, aged, and measured as per the standard operating procedure (SOP) of the Gujarat Forest Department, Government of Gujarat, and recorded the data in the trapping datasheet. The radio-collars were deployed considering the neck girth of the individual, ensuring free movement of it so as not to hamper the individual’s routine activities. After deploying the radio-collar, we used the specific antidote for Xylazine, i.e., Yohimbine hydrochloride (0.1–0.15 mg per kg body weight; Yohimbe, Equimed, USA) intravenously, resulting in the total recovery of immobilized individuals32 within 5–10 min. The individuals were intensively monitored for 72 h and, after that, regularly monitored throughout the functional period of the radio-collars. The entire radio-collaring exercise was carried out by trained and experienced veterinary officers and their teams that constituted wildlife health care personnel and field staff.Each collar had a unique VHF and UHF frequency. The radio-collars were equipped with a programmable GPS schedule and configured to record the location fixes at every hour and provided the data through the constellation of low-earth-orbit Iridium satellite data service (Iridium Communications Inc., Virginia, USA) at four-hour intervals after getting activated. The data logs included location fixes in degree decimal format (latitude/longitude), speed (km/hour), altitude (meters above mean sea level), UTC timestamp (dd-mm-yyyy h:m:s), direction (degrees), and temperature (Celsius). Radio-collars were equipped with mortality sensors and a programmable drop-off activation system. Gir Hi-Tech Monitoring Unit, Sasan-Gir, Gujarat, monitored and coordinated these activities. The location data from each radio-collar was downloaded using the GPS Plus X software (Vectronics Aerospace GmbH, Berlin, Germany) in the Gir Hi-Tech Monitoring Unit (a technology-driven scientific monitoring initiative in the landscape established in 2019 at Sasan-Gir, Gujarat).Data analysisIn this study, we calculated the home range of lions resident in the coastal region using the Fixed Kernel method. We expressed them as 90% and 50% Fixed Kernel (FK) to summarize the overall home range and core area, respectively35,36,37. Additionally, the home range of lions categorized as “link lions” and lions of the protected area was summarized for comparison (Table 1).MaxEnt (version 3.4.1) stand-alone software38 was applied for fine-scaled lion distribution modelling39,40. The logistic output format was set for the MaxEnt output. 30% random lion occurrence points were used as test data to evaluate model performance. The area under the receiver operating characteristic curve (AUC) was used to evaluate the discriminative ability of the model based on the values of sensitivity (correct discrimination of true positive location points) and specificity (correct discrimination of true negative absence points)41. The Jackknife regularised training gain for the species was used to understand the effect of each variable in model building. The logical output by the MaxEnt was presented in a table format as “percent contribution” and “permutation importance” values (from 0 to 100%). Spatial inputs were prepared on the GIS platform using ArcMap (version 10.8.1, ESRI, Redlands, USA)42. Input data for MaxEnt were categorized as (i) lion occurrence data, (ii) model variables were prepared as described below:

    i.

    Occurrence data
    At the first level, inconsistent location fixes (records with missing coordinates, time stamps, and elevation) and outliers were filtered out. Next, each lion’s hourly GPS location fixes obtained from remotely monitored radio-telemetry data were randomized to overcome spatial and temporal biases. The data was reduced by taking every three-hour location fix43,44. The data was further categorized season-wise, viz. summer, monsoon and winter. This consolidated data was then subject to spatial thinning of one kilometre using SDMtoolbox (version 2.0)45,46.

    ii.

    Model variables

    The variables used for distribution modelling broadly included different categories of land use, including both natural habitats and anthropogenic factors, namely, roads and human settlement areas. All variables were rasterized at 10 m spatial resolution.Land Use Land Cover (LULC) data of Saurashtra was obtained from Bhaskaracharya National Institute for Space Applications and Geo-informatics (BISAG-N), Gandhinagar, Gujarat. The data was then further classified into 18 sub-classes—Forest, Sandy areas, Salt-affected, Saltpan, open scrub, dense scrub (Wastelands), Waterlogged, River/Stream/Drain, Lakes and Ponds, Mining/Industrial areas, Reservoir/Tanks, Mangrove/Swamp Area, Crop Land, Agriculture Plantation (horticulture and agro-forestry), Core urban, Mixed settlement, Peri-urban, Village (Fig. 2).Roads and highways were also analyzed as separate variables in the model. Roads were classified as village roads, major district roads, and state and national highways and digitized individually to estimate Euclidean distance further (Table 2). Euclidean distance from the human settlement (Core-urban, Peri-urban, villages and mixed settlement) was analyzed and taken as a separate input variable for the model. More

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    Sugarcane cultivation practices modulate rhizosphere microbial community composition and structure

    Meghana, M. & Shastri, Y. Sustainable valorization of sugar industry waste: Status, opportunities, and challenges. Biores. Technol. 303, 122929 (2020).CAS 

    Google Scholar 
    Petrescu, D. C., Vermeir, I. & Petrescu-Mag, R. M. Consumer understanding of food quality, healthiness, and environmental impact: a cross-national perspective. IJERPH 17, 169 (2019).PubMed Central 

    Google Scholar 
    Kassam, A., Friedrich, T., Shaxson, F. & Pretty, J. The spread of conservation agriculture: justification, sustainability and uptake. Int. J. Agric. Sustain. 7, 292–320 (2009).
    Google Scholar 
    Malviya, M. K. et al. Sugarcane microbiome: role in sustainable production. In Microbiomes and Plant Health 225–242 (Elsevier, 2021). https://doi.org/10.1016/B978-0-12-819715-8.00007-0.Chapter 

    Google Scholar 
    Sandhu, H. S., Wratten, S. D. & Cullen, R. Organic agriculture and ecosystem services. Environ. Sci. Policy 13, 1–7 (2010).CAS 

    Google Scholar 
    Schipanski, M. E. et al. Balancing multiple objectives in organic feed and forage cropping systems. Agr. Ecosyst. Environ. 239, 219–227 (2017).
    Google Scholar 
    Knapp, S. & van der Heijden, M. G. A. A global meta-analysis of yield stability in organic and conservation agriculture. Nat. Commun. 9, 3632 (2018).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bender, S. F., Wagg, C. & van der Heijden, M. G. A. An underground revolution: biodiversity and soil ecological engineering for agricultural sustainability. Trends Ecol. Evol. 31, 440–452 (2016).PubMed 

    Google Scholar 
    Berendsen, R. L., Pieterse, C. M. J. & Bakker, P. A. H. M. The rhizosphere microbiome and plant health. Trends Plant Sci. 17, 478–486 (2012).CAS 
    PubMed 

    Google Scholar 
    Chialva, M., Lanfranco, L. & Bonfante, P. The plant microbiota: composition, functions, and engineering. Curr. Opin. Biotechnol. 73, 135–142 (2022).CAS 
    PubMed 

    Google Scholar 
    Dastogeer, K. M. G., Tumpa, F. H., Sultana, A., Akter, M. A. & Chakraborty, A. Plant microbiome–an account of the factors that shape community composition and diversity. Curr. Plant Biol. 23, 100161 (2020).
    Google Scholar 
    Yang, B., Wang, Y. & Qian, P.-Y. Sensitivity and correlation of hypervariable regions in 16S rRNA genes in phylogenetic analysis. BMC Bioinformat. 17, 135 (2016).
    Google Scholar 
    Nilsson, R. H. et al. The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res. 47, D259–D264 (2019).CAS 
    PubMed 

    Google Scholar 
    Wright, R. J., Gibson, M. I. & Christie-Oleza, J. A. Understanding microbial community dynamics to improve optimal microbiome selection. Microbiome 7, 85 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    Praeg, N. & Illmer, P. Microbial community composition in the rhizosphere of Larix decidua under different light regimes with additional focus on methane cycling microorganisms. Sci. Rep. 10, 22324 (2020).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    de Souza, R. S. C. et al. Unlocking the bacterial and fungal communities assemblages of sugarcane microbiome. Sci. Rep. 6, 28774 (2016).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Tayyab, M. et al. Sugarcane cultivars manipulate rhizosphere bacterial communities’ structure and composition of agriculturally important keystone taxa. 3 Biotech. 12, 32 (2022).PubMed 

    Google Scholar 
    Tayyab, M. et al. Sugarcane cultivar-dependent changes in assemblage of soil rhizosphere fungal communities in subtropical ecosystem. Environ. Sci. Pollut. Res. 29, 20795–20807 (2022).
    Google Scholar 
    Dakora, F. D., Matiru, V. N. & Kanu, A. S. Rhizosphere ecology of lumichrome and riboflavin, two bacterial signal molecules eliciting developmental changes in plants. Front. Plant Sci. 6, 700 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    Chapelle, E., Mendes, R., Bakker, P. A. H. & Raaijmakers, J. M. Fungal invasion of the rhizosphere microbiome. ISME J. 10, 265–268 (2016).CAS 
    PubMed 

    Google Scholar 
    Teheran-Sierra, L. G. et al. Bacterial communities associated with sugarcane under different agricultural management exhibit a diversity of plant growth-promoting traits and evidence of synergistic effect. Microbiol. Res. 247, 126729 (2021).CAS 
    PubMed 

    Google Scholar 
    de Carvalho, L. A. L. et al. Farming systems influence the compositional, structural, and functional characteristics of the sugarcane-associated microbiome. Microbiol. Res. 252, 126866 (2021).PubMed 

    Google Scholar 
    Henneron, L. et al. Fourteen years of evidence for positive effects of conservation agriculture and organic farming on soil life. Agron. Sustain. Dev. 35, 169–181 (2015).
    Google Scholar 
    Hartmann, M., Frey, B., Mayer, J., Mäder, P. & Widmer, F. Distinct soil microbial diversity under long-term organic and conventional farming. ISME J. 9, 1177–1194 (2015).PubMed 

    Google Scholar 
    Tayyab, M. et al. Sugarcane monoculture drives microbial community composition, activity and abundance of agricultural-related microorganisms. Environ. Sci. Pollut. Res. 28, 48080–48096 (2021).CAS 

    Google Scholar 
    Pang, Z. et al. Soil Metagenomics reveals effects of continuous sugarcane cropping on the structure and functional pathway of rhizospheric microbial community. Front. Microbiol. 12, 627569 (2021).PubMed 
    PubMed Central 

    Google Scholar 
    Orr, C. H., Stewart, C. J., Leifert, C., Cooper, J. M. & Cummings, S. P. Effect of crop management and sample year on abundance of soil bacterial communities in organic and conventional cropping systems. J. Appl. Microbiol. 119, 208–214 (2015).CAS 
    PubMed 

    Google Scholar 
    Brasil. Lei no 10.831, de 23 de dezembro de 2003. Dispõe sobre a agricultura orgânica e dá outras providências. In Publicado no Diário Oficial da União de 24/12/2003 (2003).Europea, C. Reglamento (CE) no 834/2007 del Consejo, de 28 de junio de 2007, sobre producción y etiquetado de los productos ecológicos y por el que se deroga el Reglamento (CEE) no 2092/91. D. Of. Unión Eur. 20, 1–23 (2007).
    Google Scholar 
    Council of the European Union. 889/2008, “Commission Regulation 889/2008/EC of 5 September 2008 laying down detailed rules for the implementation of Council Regulation (EC) No 834/2007 on organic production and labelling of organic products with regard to organic production, labelling and control”. Off. J. Eur. Union (L) 250, 18–19 (2007).
    Google Scholar 
    de Andrade, J. C., Cantarella, H. & Quaggio, J. A. Análise química para avaliação da fertilidade de solos tropicais. (2001).Donagema, G. K., de Campos, D. B., Calderano, S. B., Teixeira, W. G. & Viana, J. M. Manual de métodos de análise de solo. In Embrapa Solos-Documentos (INFOTECA-E) (2011).Kassambara, A. ggpubr: ‘ggplot2’ Based Publication Ready Plots. (2020). at R Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2020). At Lundberg, D. S., Yourstone, S., Mieczkowski, P., Jones, C. D. & Dangl, J. L. Practical innovations for high-throughput amplicon sequencing. Nat. Methods 10, 999–1002 (2013).CAS 
    PubMed 

    Google Scholar 
    Fadrosh, D. W. et al. An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome 2, 6 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    Renaud, G., Stenzel, U., Maricic, T., Wiebe, V. & Kelso, J. deML: robust demultiplexing of Illumina sequences using a likelihood-based approach. Bioinformatics 31, 770–772 (2015).CAS 
    PubMed 

    Google Scholar 
    Zhang, J., Kobert, K., Flouri, T. & Stamatakis, A. PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 30, 614–620 (2014).CAS 
    PubMed 

    Google Scholar 
    Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).CAS 
    PubMed 

    Google Scholar 
    Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581 (2016).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Cole, J. R. et al. Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res. 42, D633–D642 (2014).CAS 
    PubMed 

    Google Scholar 
    McMurdie, P. J. & Holmes, S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8, e61217 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lahti, L. & Shetty, S. Microbiome R package. (2012).Oksanen, J. et al. vegan: Community Ecology Package. (2019). At Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    Dhariwal, A. et al. MicrobiomeAnalyst: a web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data. Nucleic Acids Res. 45, W180–W188 (2017).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Douglas, G. M. et al. PICRUSt2: an improved and extensible approach for metagenome inference. Bioinformatics https://doi.org/10.1101/672295 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Parks, D. H., Tyson, G. W., Hugenholtz, P. & Beiko, R. G. STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30, 3123–3124 (2014).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kohl, M., Wiese, S. & Warscheid, B. Cytoscape: software for visualization and analysis of biological networks. In Data Mining in Proteomics (eds Hamacher, M. et al.) 291–303 (Humana Press, Totowa, NJ, 2011). https://doi.org/10.1007/978-1-60761-987-1_18.Chapter 

    Google Scholar 
    Assenov, Y., Ramírez, F., Schelhorn, S.-E., Lengauer, T. & Albrecht, M. Computing topological parameters of biological networks. Bioinformatics 24, 282–284 (2008).CAS 
    PubMed 

    Google Scholar 
    Shen, Z. et al. Deep 16S rRNA pyrosequencing reveals a bacterial community associated with banana fusarium wilt disease suppression induced by bio-organic fertilizer application. PLoS One 9, e98420 (2014).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Yun, Y. et al. The relationship between pH and bacterial communities in a single karst ecosystem and its implication for soil acidification. Front. Microbiol. 7, 1955 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Wu, Y., Zeng, J., Zhu, Q., Zhang, Z. & Lin, X. pH is the primary determinant of the bacterial community structure in agricultural soils impacted by polycyclic aromatic hydrocarbon pollution. Sci. Rep. 7, 40093 (2017).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Li, R. et al. Pyrosequencing reveals the influence of organic and conventional farming systems on bacterial communities. PLoS One 7, e51897 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bill, M., Chidamba, L., Gokul, J. K., Labuschagne, N. & Korsten, L. Bacterial community dynamics and functional profiling of soils from conventional and organic cropping systems. Appl. Soil. Ecol. 157, 103734 (2021).
    Google Scholar 
    Xun, W., Shao, J., Shen, Q. & Zhang, R. Rhizosphere microbiome: Functional compensatory assembly for plant fitness. Comput. Struct. Biotechnol. J. 19, 5487–5493 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Semenov, M. V., Krasnov, G. S., Semenov, V. M. & van Bruggen, A. Mineral and organic fertilizers distinctly affect fungal communities in the crop rhizosphere. JoF 8, 251 (2022).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wang, Z., Li, Y., Li, T., Zhao, D. & Liao, Y. Tillage practices with different soil disturbance shape the rhizosphere bacterial community throughout crop growth. Soil Tillage Res. 197, 104501 (2020).
    Google Scholar 
    Gdanetz, K. & Trail, F. The wheat microbiome under four management strategies, and potential for endophytes in disease protection. Phytobiom. J. 1, 158–168 (2017).
    Google Scholar 
    Lazcano, C. et al. The rhizosphere microbiome plays a role in the resistance to soil-borne pathogens and nutrient uptake of strawberry cultivars under field conditions. Sci. Rep. 11, 3188 (2021).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Leys, N. M. E. J. et al. Occurrence and phylogenetic diversity of Sphingomonas strains in soils contaminated with polycyclic aromatic hydrocarbons. Appl. Environ. Microbiol. 70, 1944–1955 (2004).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Yin, C. et al. Role of bacterial communities in the natural suppression of rhizoctonia solani bare patch disease of wheat (Triticum aestivum L.). Appl. Environ. Microbiol. 79, 7428–7438 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Stewart, A. & Hill, R. Applications of trichoderma in plant growth promotion. In Biotechnology and Biology of Trichoderma 415–428 (Elsevier, 2014). https://doi.org/10.1016/B978-0-444-59576-8.00031-X.Chapter 

    Google Scholar 
    Banerjee, S. et al. Network analysis reveals functional redundancy and keystone taxa amongst bacterial and fungal communities during organic matter decomposition in an arable soil. Soil Biol. Biochem. 97, 188–198 (2016).CAS 

    Google Scholar 
    Andargie, M., Congyi, Z., Yun, Y. & Li, J. Identification and evaluation of potential bio-control fungal endophytes against Ustilagonoidea virens on rice plants. World J. Microbiol. Biotechnol. 33, 120 (2017).PubMed 

    Google Scholar 
    Orrù, L. et al. How tillage and crop rotation change the distribution pattern of fungi. Front. Microbiol. 12, 634325 (2021).PubMed 
    PubMed Central 

    Google Scholar 
    van der Heijden, M. G. A. & Hartmann, M. Networking in the plant microbiome. PLoS Biol. 14, e1002378 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Wang, W. et al. Consistent responses of the microbial community structure to organic farming along the middle and lower reaches of the Yangtze River. Sci. Rep. 6, 35046 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Silva, T. M. et al. Degradation of 2,4-D herbicide by microorganisms isolated from Brazilian contaminated soil. Braz. J. Microbiol. 38, 522–525 (2007).
    Google Scholar 
    Laura, M., Snchez-Salinas, E., Gonzlez, E. D. & Luisa, M. Pesticide biodegradation: mechanisms, genetics and strategies to enhance the process. In Biodegradation – Life of Science (ed. Chamy, R.) (InTech, 2013). https://doi.org/10.5772/56098.Chapter 

    Google Scholar 
    Upadhyay, L. S. B. & Dutt, A. Microbial detoxification of residual organophosphate pesticides in agricultural practices. In Microbial Biotechnology (eds Patra, J. K. et al.) 225–242 (Springer Singapore, Singapore, 2017). https://doi.org/10.1007/978-981-10-6847-8_10.Chapter 

    Google Scholar 
    Hassan, Y. I., Lepp, D., He, J. & Zhou, T. Draft genome sequences of Devosia sp. strain 17-2-E-8 and Devosia riboflavina strain IFO13584. Genome Announ. https://doi.org/10.1128/genomeA.00994-14 (2014).Article 

    Google Scholar 
    Talwar, C. et al. Defining the environmental adaptations of genus Devosia: insights into its expansive short peptide transport system and positively selected genes. Sci. Rep. 10, 1151 (2020).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Li, F., Chen, L., Zhang, J., Yin, J. & Huang, S. Bacterial community structure after long-term organic and inorganic fertilization reveals important associations between soil nutrients and specific taxa involved in nutrient transformations. Front. Microbiol. 8, 187 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Ho, A., Lonardo, D. P. D. & Bodelier, P. L. E. Revisiting life strategy concepts in environmental microbial ecology. Microbiol. Ecol. https://doi.org/10.1093/femsec/fix006 (2017).Article 

    Google Scholar 
    Lupatini, M., Korthals, G. W., de Hollander, M., Janssens, T. K. S. & Kuramae, E. E. Soil microbiome is more heterogeneous in organic than in conventional farming system. Front. Microbiol. 7, 2064 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Wang, H. et al. Eight years of manure fertilization favor copiotrophic traits in paddy soil microbiomes. Eur. J. Soil Biol. 106, 103352 (2021).CAS 

    Google Scholar 
    Fließbach, A., Oberholzer, H.-R., Gunst, L. & Mäder, P. Soil organic matter and biological soil quality indicators after 21 years of organic and conventional farming. Agric. Ecosyst. Environ. 118, 273–284 (2007).
    Google Scholar 
    Lewin, G. R. et al. Evolution and ecology of Actinobacteria and their bioenergy applications. Annu. Rev. Microbiol. 70, 235–254 (2016).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Karanja, E. N. et al. Diversity and structure of prokaryotic communities within organic and conventional farming systems in central highlands of Kenya. PLoS One 15, e0236574 (2020).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Francioli, D. et al. Mineral versus organic amendments: microbial community structure, activity and abundance of agriculturally relevant microbes are driven by long-term fertilization strategies. Front. Microbiol. 7, 1446 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Paungfoo-Lonhienne, C. et al. Nitrogen fertilizer dose alters fungal communities in sugarcane soil and rhizosphere. Sci. Rep. 5, 8678 (2015).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Pang, Z. et al. Liming positively modulates microbial community composition and function of sugarcane fields. Agronomy 9, 808 (2019).CAS 

    Google Scholar 
    Aira, M., Gómez-Brandón, M., Lazcano, C., Bååth, E. & Domínguez, J. Plant genotype strongly modifies the structure and growth of maize rhizosphere microbial communities. Soil Biol. Biochem. 42, 2276–2281 (2010).CAS 

    Google Scholar 
    Ma, M. et al. Responses of fungal community composition to long-term chemical and organic fertilization strategies in Chinese Mollisols. MicrobiologyOpen 7, e00597 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    Bellenger, J. P., Darnajoux, R., Zhang, X. & Kraepiel, A. M. L. Biological nitrogen fixation by alternative nitrogenases in terrestrial ecosystems: a review. Biogeochemistry 149, 53–73 (2020).
    Google Scholar 
    Schmidt, J. E. et al. Effects of agricultural management on rhizosphere microbial structure and function in processing tomato plants. Appl. Environ. Microbiol. https://doi.org/10.1128/AEM.01064-19 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Agler, M. T. et al. Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLoS Biol. 14, e1002352 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Lin, Y. et al. Nitrosospira cluster 8a plays a predominant role in the nitrification process of a subtropical Ultisol under long-term inorganic and organic fertilization. Appl. Environ. Microbiol. 84, e01031-e1118 (2018).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Chu, H. et al. Community structure of ammonia-oxidizing bacteria under long-term application of mineral fertilizer and organic manure in a sandy loam soil. Appl. Environ. Microbiol. 73, 485–491 (2007).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Xun, W. et al. Specialized metabolic functions of keystone taxa sustain soil microbiome stability. Microbiome 9, 35 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar  More

  • in

    Site-specific temporal variation of population dynamics in subalpine endemic plant species

    Theurillat, J.-P. & Guisan, A. Potential impact of climate change on vegetation in the European Alps: A review. Clim. Change 50, 77–109 (2001).CAS 

    Google Scholar 
    Diaz, H. F. & Eischeid, J. K. Disappearing “alpine tundra” Köppen climatic type in the western United States. Geophys. Res. Lett. 34, L18707 (2007).ADS 

    Google Scholar 
    Dirnböck, T., Essl, F. & Rabitsch, W. Disproportional risk for habitat loss of high-altitude endemic species under climate change. Glob. Change Biol. 17, 990–996 (2011).ADS 

    Google Scholar 
    Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A. & Kent, J. Biodiversity hotspots for conservation priorities. Nature 403, 853–858 (2000).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Pauli, H., Gottfried, M., Dirnböck, T., Dullinger, S. & Grabherr, G. Assessing the long-term dynamics of endemic plants at summit habitats. In Alpine Biodiversity in Europe (eds. Nagy, L., Grabherr, G., Körner, C., & Thompson, D. B.) 195–207 (Springer, 2003).Cogoni, D., Sulis, E., Bacchetta, G. & Fenu, G. The unpredictable fate of the single population of a threatened narrow endemic Mediterranean plant. Biodivers. Conserv. 28, 1799–1813 (2019).
    Google Scholar 
    Cursach, J., Besnard, A., Rita, J. & Fréville, H. Demographic variation and conservation of the narrow endemic plant Ranunculus weyleri. Acta Oecol. 53, 102–109 (2013).ADS 

    Google Scholar 
    Dibner, R. R., DeMarche, M. L., Louthan, A. M. & Doak, D. F. Multiple mechanisms confer stability to isolated populations of a rare endemic plant. Ecol. Monogr. 89, e01360 (2019).
    Google Scholar 
    Boyce, M. S., Haridas, C. V., Lee, C. T., NCEAS Stochastic Demography Working Group. Demography in an increasingly variable world. Trends Ecol. Evol. 21, 141–148 (2006).PubMed 

    Google Scholar 
    Buckley, Y. M. et al. Causes and consequences of variation in plant population growth rate: A synthesis of matrix population models in a phylogenetic context. Ecol. Lett. 13, 1182–1197 (2010).PubMed 

    Google Scholar 
    Abbott, R. E., Doak, D. F. & DeMarche, M. L. Portfolio effects, climate change, and the persistence of small populations: Analyses on the rare plant Saussurea weberi. Ecology 98, 1071–1081 (2017).PubMed 

    Google Scholar 
    Villellas, J., Doak, D. F., García, M. B. & Morris, W. F. Demographic compensation among populations: What is it, how does it arise and what are its implications?. Ecol. Lett. 18, 1139–1152 (2015).PubMed 

    Google Scholar 
    Doak, D. F. & Morris, W. F. Demographic compensation and tipping points in climate-induced range shifts. Nature 467, 959–962 (2010).ADS 
    CAS 
    PubMed 

    Google Scholar 
    García-Camacho, R., Albert, M. J. & Escudero, A. Small-scale demographic compensation in a high-mountain endemic: The low edge stands still. Plant Ecol. Divers. 5, 37–44 (2012).
    Google Scholar 
    Andrello, M. et al. Accounting for stochasticity in demographic compensation along the elevational range of an alpine plant. Ecol. Lett. 23, 870–880 (2020).PubMed 

    Google Scholar 
    Valladares, F. et al. The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change. Ecol. Lett. 17, 1351–1364 (2014).PubMed 

    Google Scholar 
    Ægisdóttir, H. H., Kuss, P. & Stöcklin, J. Isolated populations of a rare alpine plant show high genetic diversity and considerable population differentiation. Ann. Bot. 104, 1313–1322 (2009).PubMed 
    PubMed Central 

    Google Scholar 
    Morente-López, J. et al. Geography and environment shape landscape genetics of Mediterranean alpine species Silene ciliata Poiret. (Caryophyllaceae). Front. Plant Sci. 9, 1698 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    Franks, S. J., Weber, J. J. & Aitken, S. N. Evolutionary and plastic responses to climate change in terrestrial plant populations. Evol. Appl. 7, 123–139 (2014).PubMed 

    Google Scholar 
    Jeong, H., Cho, Y.-C. & Kim, E. Differential plastic responses to temperature and nitrogen deposition in the subalpine plant species, Primula farinosa subsp. modesta. AoB Plants 13, plab061 (2021).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sulis, E., Bacchetta, G., Cogoni, D. & Fenu, G. From global to local scale: Where is the best for conservation purpose?. Biodivers. Conserv. 30, 183–200 (2021).
    Google Scholar 
    Hambler, D. & Dixon, J. Primula farinosa L. J. Ecol. 91, 694–705 (2003).
    Google Scholar 
    Arnold, E. & Richards, A. On the occurrence of unilateral incompatibility in Primula section Aleuritia Duby and the origin of Primula scotica Hook. Bot. J. Linn. Soc. 128, 359–368 (1998).
    Google Scholar 
    Tribsch, A. Areas of endemism of vascular plants in the eastern Alps in relation to Pleistocene glaciation. J. Biogeogr. 31, 747–760 (2004).
    Google Scholar 
    Chung, J.-M., Son, S.-W., Kim, S.-Y., Park, G.-W. & Kim, S.-S. Genetic diversity and geographic differentiation in the endangered Primula farinosa subsp. modesta, a subalpine endemic to Korea. Korean J. Plant. Taxon. 43, 236–243 (2013).
    Google Scholar 
    Lindborg, R. & Ehrlén, J. Evaluating the extinction risk of a perennial herb: Demographic data versus historical records. Conserv. Biol. 16, 683–690 (2002).
    Google Scholar 
    Caswell, H. Matrix Population Models, 2nd ed (Sinauer Associates Inc, 2000).Salguero-Gómez, R. & De Kroon, H. Matrix projection models meet variation in the real world. J. Ecol. 98, 250–254 (2010).
    Google Scholar 
    Jongejans, E. et al. Region versus site variation in the population dynamics of three short-lived perennials. J. Ecol. 98, 279–289 (2010).
    Google Scholar 
    Jongejans, E. & De Kroon, H. Space versus time variation in the population dynamics of three co-occurring perennial herbs. J. Ecol. 93, 681–692 (2005).
    Google Scholar 
    Suggitt, A. J. et al. Habitat microclimates drive fine-scale variation in extreme temperatures. Oikos 120, 1–8 (2011).
    Google Scholar 
    Tomimatsu, H. & Ohara, M. Demographic response of plant populations to habitat fragmentation and temporal environmental variability. Oecologia 162, 903–911 (2010).ADS 
    PubMed 

    Google Scholar 
    Kudernatsch, T., Fischer, A., Bernhardt-Römermann, M. & Abs, C. Short-term effects of temperature enhancement on growth and reproduction of alpine grassland species. Basic Appl. Ecol. 9, 263–274 (2008).
    Google Scholar 
    Kim, E. & Donohue, K. Local adaptation and plasticity of Erysimum capitatum to altitude: Its implications for responses to climate change. J. Ecol. 101, 796–805 (2013).
    Google Scholar 
    Forbis, T. A. Seedling demography in an alpine ecosystem. Am. J. Bot. 90, 1197–1206 (2003).PubMed 

    Google Scholar 
    Yenni, G., Adler, P. B. & Ernest, S. M. Strong self-limitation promotes the persistence of rare species. Ecology 93, 456–461 (2012).PubMed 

    Google Scholar 
    Doak, D. F. Source-sink models and the problem of habitat degradation: General models and applications to the Yellowstone grizzly. Conserv. Biol. 9, 1370–1379 (1995).
    Google Scholar 
    Lesica, P. & Crone, E. E. Arctic and boreal plant species decline at their southern range limits in the Rocky Mountains. Ecol. Lett. 20, 166–174 (2017).PubMed 

    Google Scholar 
    Oldfather, M. F. & Ackerly, D. D. Microclimate and demography interact to shape stable population dynamics across the range of an alpine plant. New Phytol. 222, 193–205 (2019).PubMed 

    Google Scholar 
    Ågren, J., Fortunel, C. & Ehrlén, J. Selection on floral display in insect-pollinated Primula farinosa: Effects of vegetation height and litter accumulation. Oecologia 150, 225–232 (2006).ADS 
    PubMed 

    Google Scholar 
    Ehrlén, J., Syrjänen, K., Leimu, R., Begona Garcia, M. & Lehtilä, K. Land use and population growth of Primula veris: An experimental demographic approach. J. Appl. Ecol. 42, 317–326 (2005).
    Google Scholar 
    Ehrlén, J. & Morris, W. F. Predicting changes in the distribution and abundance of species under environmental change. Ecol. Lett. 18, 303–314 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    Stubben, C. & Milligan, B. Estimating and analyzing demographic models using the popbio package in R. J. Stat. Softw. 22, 1–23 (2007).
    Google Scholar 
    Weiss, N. Package ‘wPerm’. https://cran.r-project.org/web/packages/wPerm/wPerm.pdf. (2015).Frossard, J. & Renaud, O. Permutation tests for regression, ANOVA, and comparison of signals: The permuco package. J. Stat. Softw. 99, 1–32 (2021).
    Google Scholar  More

  • in

    Acoustic and visual cetacean surveys reveal year-round spatial and temporal distributions for multiple species in northern British Columbia, Canada

    Williams, R. et al. Prioritizing global marine mammal habitats using density maps in place of range maps. Ecography 37, 212–220 (2014).
    Google Scholar 
    Tyack, P. L. & Clark, C. W. Communication and acoustic behavior of dolphins and whales in Hearing by whales and dolphins 156–224 (Springer, 2000).Davis, G. E. et al. Exploring movement patterns and changing distributions of baleen whales in the western North Atlantic using a decade of passive acoustic data. Glob. Change Biol. 26, 4812 (2020).ADS 

    Google Scholar 
    Lomac-MacNair, K. S. et al. Marine mammal visual and acoustic surveys near the Alaskan Colville River Delta. Polar Biol. 42, 441–448 (2018).
    Google Scholar 
    Keen, E., Hendricks, B., Wray, J., Alidina, H. & Picard, C. Integrating passive acoustic and visual surveys for marine mammals in coastal habitats in 176th Meeting of Acoustical Society of America. 1 edn.Gregr, E. J., Baumgartner, M. F., Laidre, K. L. & Palacios, D. M. Marine mammal habitat models come of age: The emergence of ecological and management relevance. Endang. Species Res. 22, 205–212 (2013).
    Google Scholar 
    Hastie, G. D., Wilson, B., Wilson, L., Parsons, K. M. & Thompson, P. M. Functional mechanisms underlying cetacean distribution patterns: Hotspots for bottlenose dolphins are linked to foraging. Mar. Biol. 144, 397–403 (2004).
    Google Scholar 
    Lambert, C., Mannocci, L., Lehodey, P. & Ridoux, V. Predicting cetacean habitats from their energetic needs and the distribution of their prey in two contrasted tropical regions. PLoS ONE 9, e105958 (2014).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Huot, Y. et al. Does chlorophyll a provide the best index of phytoplankton biomass for primary productivity studies?. Biogeosci. Discuss. 4, 707–745 (2007).ADS 

    Google Scholar 
    Etnoyer, P. et al. Sea-surface temperature gradients across blue whale and sea turtle foraging trajectories off the Baja California Peninsula, Mexico. Deep Sea Res. II 53, 340–358 (2006).ADS 

    Google Scholar 
    Shabangu, F. W. et al. Seasonal occurrence and diel calling behaviour of Antarctic blue whales and fin whales in relation to environmental conditions off the west coast of South Africa. J. Mar. Syst. 190, 25–39 (2019).
    Google Scholar 
    Haida Nation & Parks Canada Agency. Gwaii Haanas Gina ’Waadluxan Kilguhlga. Land-Sea-People Management Plan. 33 (© Council of the Haida Nation and Her Majesty the Queen in Right of Canada, represented by the Chief Executive Officer of Parks Canada, 2018).Ford, J. K. B. Marine Mammals of British Columbia. (Royal BC Museum, 2014).Allen, A. S., Yurk, H., Vagle, S., Pilkington, J. & Canessa, R. The underwater acoustic environment at SGaan Kinghlas-Bowie Seamount Marine Protected Area: Characterizing vessel traffic and associated noise using satellite AIS and acoustic datasets. Mar. Pollut. Bull. 128, 82–88 (2018).CAS 
    PubMed 

    Google Scholar 
    Ainslie, M. A. Principles of Sonar Performance Modeling. (Springer, 2010).Collins, M. D. A split-step Padé solution for the parabolic equation method. J. Acoust. Soc. Am. 93, 1736–1742 (1993).ADS 

    Google Scholar 
    Porter, M. B. & Bucker, H. P. Gaussian beam tracing for computing ocean acoustic fields. J. Acoust. Soc. Am. 82, 1349–1359 (1987).ADS 

    Google Scholar 
    Mouy, X., MacGillivray, A. O., Vallarta, J. H., Martin, B. & Delarue, J. J.-Y. Ambient Noise and Killer Whale Monitoring near Port Metro Vancouver’s Proposed Terminal 2 Expansion Site: July–September 2012. (Technical report by JASCO Applied Sciences for Hemmera, 2012).Ford, J. et al. Distribution and relative abundance of cetaceans in western Canadian waters from ship surveys, 2002–2008. Can. Tech. Rep. Fish. Aquat. Sci. 2913, 51 (2010).
    Google Scholar 
    Wright, B. M., Nichol, L. M. & Doniol-Valcroze, T. Spatial density models of cetaceans in the Canadian Pacific estimated from 2018 ship-based surveys. DFO Can. Sci. Advis. Sec. Res. Doc. 2021, 49 (2021).
    Google Scholar 
    Devred, E., Hardy, M. & Hannah, C. Satellite observations of the Northeast Pacific Ocean. Can. Tech. Rep. Hydrogr. Ocean Sci. 335, 46 (2021).
    Google Scholar 
    Saha, K. et al. NOAA National centers for environmental information. Dataset https://doi.org/10.7289/v52j68xx (2018).Article 

    Google Scholar 
    NASA Goddard Space Flight Center, Ocean Ecology Laboratory & Ocean Biology Processing Group. (NASA OB.DAAC, Greenbelt, MD, USA. https://doi.org/10.5067/AQUA/MODIS/L3B/CHL/2018. Accessed 3 Feb 2021.Wood, S. N. Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J. R. Stat. Soc. B Stat. Methodol. 73, 3–36 (2011).MathSciNet 
    MATH 

    Google Scholar 
    R Core Team. R: A language and environment for statistical computing. R foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (2021).Ogle, D. H., Wheeler, P. & Dinno, A. FSA: Fisheries Stock Analysis. R package version 0.8.32. https://github.com/droglenc/FSA (2021).Payne, R. S. & McVay, S. Songs of humpback whales. Science 173, 585–597 (1971).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Rekdahl, M. L. et al. Non-song social call bouts of migrating humpback whales. J. Acoust. Soc. Am. 137, 3042–3053 (2015).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Oswald, J. N., Rankin, S. & Barlow, J. To whistle or not to whistle? Geographic variation in the whistling behavior of small odontocetes. Aquat. Mamm. 34, 288–302 (2008).
    Google Scholar 
    Rankin, S., Oswald, J., Barlow, J. P. & Lammers, M. Patterned burst-pulse vocalizations of the northern right whale dolphin, Lissodelphis borealis. J. Acoust. Soc. Am. 121, 1213–1218. https://doi.org/10.1121/1.2404919 (2007).Article 
    ADS 
    PubMed 

    Google Scholar 
    Arranz, P. et al. Discrimination of fast click-series produced by tagged Risso’s dolphins (Grampus griseus) for echolocation or communication. J. Exp. Biol. 219, 2898–2907. https://doi.org/10.1242/jeb.144295 (2016).Article 
    CAS 
    PubMed 

    Google Scholar 
    Halpin, L. R., Towers, J. R. & Ford, J. K. First record of common bottlenose dolphin (Tursiops truncatus) in Canadian Pacific waters. Mar. Biodivers. Rec. 11, 1–5 (2018).
    Google Scholar 
    Nikolich, K. & Towers, J. R. Vocalizations of common minke whales (Balaenoptera acutorostrata) in an eastern North Pacific feeding ground. Bioacoustics 29, 97–108 (2020).
    Google Scholar 
    Money, J. H. & Trites, A. W. A preliminary assessment of the status of marine mammal populations and associated research needs for the west coast of Canada. Report No. Final Report, 80 (Fisheries and Oceans Canada, 1998).Gregr, E. J. & Trites, A. W. Predictions of critical habitat for five whale species in the waters of coastal British Columbia. Can. J. Fish. Aquat. Sci. 58, 1265–1285 (2001).
    Google Scholar 
    Ou, H., Au, W. W. L., Van Parijs, S., Oleson, E. M. & Rankin, S. Discrimination of frequency-modulated Baleen whale downsweep calls with overlapping frequencies. J. Acoust. Soc. Am. 137, 3024–3032. https://doi.org/10.1121/1.4919304 (2015).Article 
    ADS 
    PubMed 

    Google Scholar 
    Mellinger, D. K., Stafford, K. M., Moore, S. E., Dziak, R. P. & Matsumoto, H. An overview of fixed passive acoustic observation methods for cetaceans. Oceanography 20, 36–45 (2007).
    Google Scholar 
    Stafford, K. M., Citta, J. J., Moore, S. E., Daher, M. A. & George, J. E. Environmental correlates of blue and fin whale call detections in the North Pacific Ocean from 1997 to 2002. Mar. Ecol. Prog. Ser. 395, 37–53 (2009).ADS 

    Google Scholar 
    Burnham, R., Duffus, D. & Mouy, X. The presence of large whale species in Clayoquot Sound and its offshore waters. Cont. Shelf Res. 177, 15–23 (2019).ADS 

    Google Scholar 
    Burtenshaw, J. C. et al. Acoustic and satellite remote sensing of blue whale seasonality and habitat in the Northeast Pacific. Deep Sea Res. II 51, 967–986 (2004).ADS 

    Google Scholar 
    Calambokidis, J., Barlow, J., Ford, J. K. B., Chandler, T. E. & Douglas, A. B. Insights into the population structure of blue whales in the Eastern North Pacific from recent sightings and photographic identification. Mar. Mamm. Sci. 25, 816–832 (2009).
    Google Scholar 
    Jackson, J. M., Thomson, R. E., Brown, L. N., Willis, P. G. & Borstad, G. A. Satellite chlorophyll off the British Columbia Coast, 1997–2010. J. Geophys. Res. Oceans 120, 4709–4728 (2015).ADS 

    Google Scholar 
    Evans, R., English, P. A., Anderson, S. C., Gauthier, S. & Robinson, C. L. Factors affecting the seasonal distribution and biomass of E. pacifica and T. spinifera along the Pacific coast of Canada: A spatiotemporal modelling approach. PLoS ONE 16, e0249818 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Moore, S. E., Watkins, W. A., Daher, M. A., Davies, J. R. & Dahlheim, M. E. Blue whale habitat associations in the Northwest Pacific: Analysis of remotely-sensed data using a Geographic Information System. Oceanography 15, 1–10 (2002).
    Google Scholar 
    Lockyer, C. Review of Baleen Whale (Mysticeti) reproduction and implications for management. Rep. Int. Whal. Commn Spec. Issue 6, 27–50 (1984).
    Google Scholar 
    Ohsumi, S. M. N. Growth of fin whale in the Northern Pacific Ocean. Sci. Rep. Whale Res. Inst. 13, 97–133 (1958).
    Google Scholar 
    Watkins, W. A. et al. Seasonality and distribution of whale calls in the North Pacific. Oceanography 13, 62–67 (2000).
    Google Scholar 
    Watkins, W. A., Tyack, P., Moore, K. E. & Bird, J. E. The 20-Hz signals of finback whales (Balaenoptera physalus). J. Acoust. Soc. Am. 82, 1901–1912 (1987).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Stafford, K. M., Mellinger, D. K., Moore, S. E. & Fox, C. G. Seasonal variability and detection range modeling of baleen whale calls in the Gulf of Alaska, 1999–2002. J. Acoust. Soc. Am. 122, 3378–3390 (2007).ADS 
    PubMed 

    Google Scholar 
    Koot, B. Winter Behaviour and Population Structure of Fin Whales (Balaenoptera physalus) in British Columbia inferred from passive acoustic data (University of British Columbia, 2015).
    Google Scholar 
    Pilkington, J. F., Stredulinsky, E. H., Abernethy, R. M. & Ford, J. K. B. Patterns of Fin whale (Balaenoptera physalus) Seasonality and Relative Distribution in Canadian Pacific Waters Inferred from Passive Acoustic Monitoring. DFO Can. Sci. Advis. Sec. Res. Doc. (2018).Best, B. D., Fox, C. H., Williams, R., Halpin, P. H. & Paquet, P. C. Updated Marine Mammal Distribution and Abundance Estimates in British Columbia (Springer, 2015).
    Google Scholar 
    Clarke, C. & Jamieson, G. Identification of ecologically and biologically significant areas in the Pacific North Coast integrated management area: Phase II: Final report. Can. Tech. Rep. Fish. Aquat. Sci. 2678, 59 (2006).
    Google Scholar 
    Nichol, L. M. et al. Distribution, movements and habitat fidelity patterns of Fin Whales (Balaenoptera physalus) in Canadian Pacific Waters. DFO Can. Sci. Advis. Sec. Res. Doc. (2018).Nichol, L. M. & Ford, J. K. B. Information in Support of the Identification of Habitat of Special Importance to Fin Whales (Balaenoptera physalus) in Canadian Pacific Waters. DFO Can. Sci. Advis. Sec. Res. Doc. (2018).Mizroch, S. A., Rice, D. W., Zwiefelhofer, D., Waite, J. & Perryman, W. L. Distribution and movements of fin whales in the North Pacific Ocean. Mammal Rev. 39, 193–227 (2009).
    Google Scholar 
    Širović, A., Williams, L. N., Kerosky, S. M., Wiggins, S. M. & Hildebrand, J. A. Temporal separation of two fin whale call types across the eastern North Pacific. Mar. Biol. 160, 47–57 (2013).PubMed 

    Google Scholar 
    Flinn, R. D., Trites, A. W., Gregr, E. J. & Perry, R. I. Diets of fin, sei, and sperm whales in British Columbia: an analysis of commercial whaling records, 1963–1967. Mar. Mamm. Sci. 18, 663–679 (2002).
    Google Scholar 
    Barnes, R. S. K. & Hughes, R. N. An Introduction to Marine Ecology (Wiley, 1999).
    Google Scholar 
    Romagosa, M. et al. Food talks: 40-hz fin whale calls are associated with prey biomass. Proc. R. Soc. B 288, 20211156 (2021).PubMed 
    PubMed Central 

    Google Scholar 
    Gregr, E. J., Nichol, L., Ford, J. K., Ellis, G. & Trites, A. W. Migration and population structure of northeastern Pacific whales off coastal British Columbia: An analysis of commercial whaling records from 1908–1967. Mar. Mamm. Sci. 16, 699–727 (2000).
    Google Scholar 
    Williams, R. & Thomas, L. Distribution and abundance of marine mammals in the coastal waters of British Columbia, Canada. J. Cetac. Res. Manage. 9, 15 (2007).
    Google Scholar 
    Dalla Rosa, L., Ford, J. K. & Trites, A. W. Distribution and relative abundance of humpback whales in relation to environmental variables in coastal British Columbia and adjacent waters. Contin. Shelf Res. 36, 89–104 (2012).ADS 

    Google Scholar 
    Winn, H. E. & Winn, L. K. The song of the humpback whale Megaptera novaeangliae in the West Indies. Mar. Biol. 47, 97–114. https://doi.org/10.1007/BF00395631 (1978).Article 

    Google Scholar 
    Baker, C. S. et al. Population characteristics and migration of summer and late-season humpback whales (Megaptera novaeangliae) in southeastern Alaska. Mar. Mamm. Sci. 1, 304–323 (1985).ADS 

    Google Scholar 
    McSweeney, D., Chu, K., Dolphin, W. & Guinee, L. North Pacific humpback whale songs: A comparison of southeast Alaskan feeding ground songs with Hawaiian wintering ground songs. Mar. Mamm. Sci. 5, 139–148 (1989).
    Google Scholar 
    Norris, T. F., McDonald, M. & Barlow, J. Acoustic detections of singing humpback whales (Megaptera novaeangliae) in the eastern North Pacific during their northbound migration. J. Acoust. Soc. Am. 106, 506–514 (1999).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Clark, C. W. & Clapham, P. J. Acoustic monitoring on a humpback whale (Megaptera novaeangliae) feeding ground shows continual singing into late spring. Proc. R. Soc. Lond. B 271, 1051–1057 (2004).
    Google Scholar 
    Stimpert, A. K., Peavey, L. E., Friedlaender, A. S. & Nowacek, D. P. Humpback whale song and foraging behavior on an Antarctic feeding ground. PLoS ONE 7, e51214 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kowarski, K., Evers, C., Moors-Murphy, H., Martin, B. & Denes, S. L. Singing through winter nights: Seasonal and diel occurrence of humpback whale (Megaptera novaeangliae) calls in and around the Gully MPA, offshore eastern Canada. Mar. Mamm. Sci. 34, 169–189 (2018).
    Google Scholar 
    Nichol, L. M., Abernethy, R., Flostrand, L., Lee, T. S. & Ford, J. K. B. Information relevant for the identification of critical habitats of north pacific humpback whales (Megaptera novaeangliae) in British Columbia. DFO Can. Sci. Advis. Sec. Res. Doc. (2010).Williams, R., Erbe, C., Ashe, E. & Clark, C. W. Quiet (er) marine protected areas. Mar. Pollut. Bull. 100, 154–161 (2015).CAS 
    PubMed 

    Google Scholar 
    Gaston, A. J., Pilgrim, N. G. & Pattison, V. Humpback Whale (Megaptera novaeangliae) observations in Laskeek Bay, western Hecate Strait, in spring and early summer, 1990–2018. Can. Field Nat. 133, 263–269 (2019).
    Google Scholar 
    Robinson, C. L., Gower, J. F. & Borstad, G. Twenty years of satellite observations describing phytoplankton blooms in seas adjacent to Gwaii Haanas National Park Reserve, Canada. Can. J. Remote Sens. 30, 36–43 (2004).ADS 

    Google Scholar 
    Swartz, S. L., Taylor, B. L. & Rugh, D. J. Gray whale Eschrichtius robustus population and stock identity. Mamm. Rev. 36, 66–84 (2006).
    Google Scholar 
    Gaston, A. J. & Heise, K. Results of cetacean observations in Laskeek Bay, 1990–2003. Laskeek Bay Res. 55, 1–10 (2004).
    Google Scholar 
    Ford, J. K. et al. New insights into the northward migration route of gray whales between Vancouver Island, British Columbia, and southeastern Alaska. Mar. Mamm. Sci. 29, 325–337 (2013).
    Google Scholar 
    Burnham, R. E. & Duffus, D. A. The use of passive acoustic monitoring as a census tool of gray whale (Eschrichtius robustus) migration. Ocean Coast. Manag. 188, 105070 (2020).
    Google Scholar 
    Best, P. B. Social organization in sperm whales. In Physeter macrocephalus in Behavior of Marine Animals (eds Winn, H. E. & Olla, B. L.) 227–289 (Springer, 1979).
    Google Scholar 
    Jaquet, N. & Gendron, D. Distribution and relative abundance of sperm whales in relation to key environmental features, squid landings and the distribution of other cetacean species in the Gulf of California, Mexico. Mar. Biol. 141, 591–601 (2002).
    Google Scholar 
    Rice, D. W. Sperm whale Physeter macrocephalus Linnaeus, 1758. Handb. Mar. Mamm. 4, 177–233 (1989).
    Google Scholar 
    Whitehead, H. & Arnbom, T. Social organization of sperm whales off the Galapagos Islands, February–April 1985. Can. J. Zool. 65, 913–919 (1987).
    Google Scholar 
    Whitehead, H. Sperm whale: Physeter macrocephalus. In Encyclopedia of Marine Mammals 3rd edn (eds Würsig, B. et al.) 919–925 (Academic Press, 2018).
    Google Scholar 
    Mizroch, S. A. & Rice, D. W. Ocean nomads: Distribution and movements of sperm whales in the North Pacific shown by whaling data and Discovery marks. Mar. Mamm. Sci. 29, E136–E165 (2013).
    Google Scholar 
    Diogou, N. et al. Sperm whale (Physeter macrocephalus) acoustic ecology at Ocean Station PAPA in the Gulf of Alaska-Part 2: Oceanographic drivers of interannual variability. Deep Sea Res. I 150, 103044 (2019).
    Google Scholar 
    Ford, J. K. & Ellis, G. M. You are what you eat: Foraging specializations and their influence on the social organization and behavior of killer whales. in Primates and Cetaceans 75–98 (Springer, 2014).Ford, J. K. B. et al. Habitats of special importance to resident killer whales (Orcinus orca) off the West Coast of Canada. DFO Can. Sci. Advis. Sec. Res. Doc. (2017).Ford, J. K. B., Stredulinsky, E. H., Ellis, G. M., Durban, J. W. & Pilkington, J. F. Offshore Killer whales in Canadian pacific waters: Distribution, seasonality, foraging ecology, population status and potential for recovery. DFO Can. Sci. Advis. Sec. Res. Doc. (2014).Nichol, L. M. & Shackleton, D. M. Seasonal movements and foraging behaviour of northern resident killer whales (Orcinus orca) in relation to the inshore distribution of salmon (Oncorhynchus spp.) in British Columbia. Can. J. Zool. 74, 983–991 (1996).
    Google Scholar 
    Olesiuk, P. F., Ellis, G. M. & Ford, J. K. Life History and Population Dynamics of Northern Resident Killer Whales (Orcinus orca) in British Columbia (Canadian Science Advisory Secretariat Ottawa, 2005).
    Google Scholar 
    Newman, K. & Springer, A. Nocturnal activity by mammal-eating killer whales at a predation hot spot in the Bering Sea. Mar. Mamm. Sci. 24, 990 (2008).
    Google Scholar 
    Ford, J. K. B. et al. Dietary specialization in two sympatric populations of killer whales (Orcinus orca) in coastal British Columbia and adjacent waters. Can. J. Zool. 76, 1456–1471 (1998).
    Google Scholar 
    Barrett-Lennard, L. G., Ford, J. K. B. & Heise, K. A. The mixed blessing of echolocation: Differences in sonar use by fish-eating and mammal-eating killer whales. Anim. Behav. 51, 553–565 (1996).
    Google Scholar 
    Deecke, V. B., Ford, J. K. B. & Slater, P. J. B. The vocal behaviour of mammal-eating killer whales: Communicating with costly calls. Anim. Behav. 69, 395–405 (2005).
    Google Scholar 
    Ford, J. K. B. Call traditions and vocal dialects of killer whales (Orcinus orca) in British Columbia Ph.D. thesis, University of British Columbia (1984).Baird, R. W. Status of killer whales, Orcinus orca, Canada. Can. Field. Nat. 115, 676–701 (2001).
    Google Scholar 
    Ford, J. K. B., Stredulinsky, E. H., Towers, J. R. & Ellis, G. M. Information in Support of the Identification of Critical Habitat for Transient Killer Whales (Orcinus orca) off the West Coast of Canada. DFO Can. Sci. Advis. Sec. Res. Doc. (2013).Tyack, P. L., Johnson, M., Soto, N. A., Sturlese, A. & Madsen, P. T. Extreme diving of beaked whales. J. Exp. Biol. 209, 4238–4253 (2006).PubMed 

    Google Scholar 
    Baumann-Pickering, S. et al. Species-specific beaked whale echolocation signals. J. Acoust. Soc. Am. 134, 2293–2301 (2013).ADS 
    PubMed 

    Google Scholar 
    Pike, G. C. Two records of Berardius bairdi from the coast of British Columbia. J. Mammal. 34, 98–104 (1953).
    Google Scholar 
    Pike, G. C. & MacAskie, I. Marine mammals of British Columbia. Fish. Res. Board Can. Bull. 171, 1–10 (1969).
    Google Scholar 
    Willis, P. M. & Baird, R. W. Sightings and strandings of beaked whales on the west coast of. Aquat. Mamm. 24, 21–25 (1998).
    Google Scholar 
    Jefferson, T. A. Phocoenoides dalli. Mamm. Spec. https://doi.org/10.2307/3504170 (1988).Article 

    Google Scholar 
    Boyd, C. et al. Estimation of population size and trends for highly mobile species with dynamic spatial distributions. Divers. Distrib. 24, 1–12 (2018).
    Google Scholar 
    Carretta, J. V., Taylor, B. L. & Chivers, S. J. Abundance and depth distribution of harbor porpoise (Phocoena phocoena) in northern California determined from a 1995 ship survey. Fish. Bull. 99, 29–29 (2001).
    Google Scholar 
    Willis, P. M. & Baird, R. W. Status of the dwarf sperm whale, Kogia simus, with special reference to Canada. Can. Field Nat. 112, 114–125 (1998).
    Google Scholar 
    Kyhn, L. A. et al. Clicking in a killer whale habitat: Narrow-band, high-frequency biosonar cliks of harbour porpoise (Phocoena phocoena) and Dall’s porpoise (Phocoenoides dalli). PLoS ONE 8, e63763 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Madsen, P., Carder, D., Bedholm, K. & Ridgway, S. Porpoise clicks from a sperm whale nose—Convergent evolution of 130 kHz pulses in toothed whale sonars?. Bioacoustics 15, 195–206 (2005).
    Google Scholar 
    Merkens, K. et al. Clicks of dwarf sperm whales (Kogia sima). Mar. Mamm. Sci. 34, 963–978 (2018).
    Google Scholar 
    Griffiths, E. T. et al. Detection and classification of narrow-band high frequency echolocation clicks from drifting recorders. J. Acoust. Soc. Am. 147, 3511–3522 (2020).ADS 
    PubMed 

    Google Scholar 
    Baird, R. W. & Stacey, P. J. Status of Risso’s Dolphin, Grampus griseus, in Canada. Naturalist 5, 233142 (1991).
    Google Scholar 
    Benoit-Bird, K. J. & Au, W. W. Prey dynamics affect foraging by a pelagic predator (Stenella longirostris) over a range of spatial and temporal scales. Behav. Ecol. Sociobiol. 53, 364–373 (2003).
    Google Scholar 
    Benoit-Bird, K. J., Würsig, B. & Mfadden, C. J. Dusky dolphin (Lagenorhynchus obscurus) foraging in two different habitats: active acoustic detection of dolphins and their prey. Mar. Mamm. Sci. 20, 215–231 (2004).
    Google Scholar 
    Soldevilla, M. S., Wiggins, S. M. & Hildebrand, J. A. Spatial and temporal patterns of Risso’s dolphin echolocation in the Southern California Bight. J. Acoust. Soc. Am. 127, 124–132 (2010).ADS 
    PubMed 

    Google Scholar 
    Soldevilla, M. S., Wiggins, S. M. & Hildebrand, J. A. Spatio-temporal comparison of Pacific white-sided dolphin echolocation click types. Aquat. Biol. 9, 49–62 (2010).
    Google Scholar 
    Taylor, F. The relationship of midwater trawl catches to sound scattering layers off the coast of northern British Columbia. J. Fish. Board Can. 25, 457–472 (1968).
    Google Scholar 
    Curtis, K. R., Howe, B. M. & Mercer, J. A. Low-frequency ambient sound in the North Pacific: Long time series observations. J. Acoust. Soc. Am. 106, 3189–3200 (1999).ADS 

    Google Scholar 
    Aroyan, J. L. et al. Acoustic models of sound production and propagation in Hearing by whales and dolphins 409–469 (Springer, 2000).
    Google Scholar 
    Cummings, W. C. & Thompson, P. O. Underwater sounds from the blue whale, Balaenoptera musculus. J. Acoust. Soc. Am. 50, 1193–1198 (1971).ADS 

    Google Scholar 
    McDonald, M. A., Calambokidis, J., Teranishi, A. M. & Hildebrand, J. A. The acoustic calls of blue whales off California with gender data. J. Acoust. Soc. Am. 109, 1728–1735 (2001).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Weirathmueller, M. J., Wilcock, W. S. D. & Soule, D. C. Source levels of fin whale 20 Hz pulses measured in the Northeast Pacific Ocean. J. Acoust. Soc. Am. 133, 741–749 (2013).ADS 
    PubMed 

    Google Scholar 
    Vihtakari, M. ggOceanMaps: Plot Data on Oceanographic Maps using ‘ggplot2’. R package version 1.2.14. https://mikkovihtakari.github.io/ggOceanMaps/ (2022). More

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    Microbiome diversity and metabolic capacity determines the trophic ecology of the holobiont in Caribbean sponges

    Gardner TA, Cote IM, Gill JA, Grant A, Watkinson AR. Long-term region-wide declines in Caribbean corals. Science. 2003;301:958–60.CAS 
    PubMed 

    Google Scholar 
    Knowlton N. The future of coral reefs. Proc Natl Acad Sci USA. 2001;98:5419–25.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Worm B, Barbier EB, Beaumont N, Duffy JE, Folke C, Halpern BS, et al. Impacts of biodiversity loss on ocean ecosystem services. Science. 2006;314:787–90.CAS 
    PubMed 

    Google Scholar 
    Dudgeon SR, Aronson RB, Bruno JF, Precht WF. Phase shifts and stable states on coral reefs. Mar Ecol Prog Ser. 2010;413:201–16.
    Google Scholar 
    Bell JJ, Davy SK, Jones T, Taylor MW, Webster NS. Could some coral reefs become sponge reefs as our climate changes? Glob Climate Change. 2013;19:2613–24.
    Google Scholar 
    McMurray SE, Henkel TP, Pawlik JR. Demographics of increasing populations of the giant barrel sponge Xestospongia muta in the Florida Keys. Ecology. 2010;91:560–70.PubMed 

    Google Scholar 
    Bell JJ. The functional roles of marine sponges. Est Coast Shelf Sci. 2008;79:341–53.
    Google Scholar 
    Lesser MP, Slattery M. Will coral reef sponges be winners in the Anthropocene? Glob Change Biol. 2020;26:3202–11.
    Google Scholar 
    Pankey MS, Plachetzki DC, Macartney KJ, Gastaldi M, Slattery M, Gochfeld DJ, et al. Co-phylogeny and convergence shape holobiont evolution in sponge-microbe symbioses. Nat Ecol Evol. 2022;6:750–62.
    Google Scholar 
    Lesser MP, Slattery M, Mobley CD. Biodiversity and functional ecology of mesophotic coral reefs. Ann Rev Ecol Syst. 2018;49:49–71.
    Google Scholar 
    Diaz MC, Rützler K. Sponges: an essential component of Caribbean coral reefs. Bull Mar Sci. 2001;69:535–46.
    Google Scholar 
    Wulff JL. Ecological interactions and the distribution, abundance, and diversity of sponges. Adv Mar Biol. 2012;61:273–344.PubMed 

    Google Scholar 
    Lesser MP. Benthic-pelagic coupling on coral reefs: feeding and growth of Caribbean sponges. J Exp Mar Biol Ecol. 2006;328:277–88.
    Google Scholar 
    Perea-Blazquez A, Davy SK, Bell JJ. Estimates of particulate organic carbon flowing from the pelagic environment to the benthos through sponge assemblages. PLoS One. 2012;7:e29569.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lesser MP, Slattery M. Ecology of Caribbean sponges: are top-down or bottom-up processes more important? PLoS One. 2013;8:e79799.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Pawlik JR. The chemical ecology of sponges on Caribbean reefs: natural products shape natural systems. BioScience. 2011;61:888–98.
    Google Scholar 
    Slattery M, Gochfeld DJ. Chemical interactions among marine competitors, and host-pathogens. In: Fattorusso, E, Gerwick, WH, Taglialatela-Scafati, O (eds). Handbook of Marine Natural Products. Springer, 2012. pp. 824–59.Thacker RW, Freeman CJ. Sponge-microbe symbioses: recent advances and new directions. Adv Mar Biol. 2012;62:57–112.PubMed 

    Google Scholar 
    Taylor MW, Radax R, Steger D, Wagner M. Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Biol Rev. 2007;71:295–347.CAS 

    Google Scholar 
    Schmitt S, Tsai P, Bell J, Fromont J, Ilan M, Lindquist N, et al. Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J. 2012;6:564–76.CAS 
    PubMed 

    Google Scholar 
    Gloeckner V, Wehrl M, Moitinho-Silva L, Gernert C, Schupp P, Pawlik JR, et al. The HMA-LMA dichotomy revisited: an electron microscopical survey of 56 sponge species. Biol Bull. 2014;227:78–88.PubMed 

    Google Scholar 
    Hentschel U, Fieseler L, Wehrl M, Gernert C, Steinert M, Hacker J, et al. Microbial diversity of marine sponges. Prog Mol Subcell Biol. 2003;37:59–88.CAS 
    PubMed 

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

    Google Scholar 
    Zhang F, Jonas L, Lin H, Hill RT. Microbially mediated nutrient cycles in marine sponges. FEMS Microbiol Ecol. 2019;95:115.
    Google Scholar 
    Schläppy M-L, Schöttner SI, Lavik G, Kuypers MMM, de Beer D, Hoffmann F. Evidence of nitrification and denitrification in high and low microbial abundance sponges. Mar Biol. 2010;157:593–602.PubMed 

    Google Scholar 
    Giles EC, Kamke J, Moitinho-Silva L, Taylor MW, Hentschel U, Ravasi T, et al. Bacterial community profiles in low microbial abundance sponges. FEMS Microbiol Ecol. 2013;83:232–41.CAS 
    PubMed 

    Google Scholar 
    Weisz JB, Lindquist N, Martens CS. Do associated microbial abundances impact marine demosponge pumping rates and tissue densities. Oecologia. 2008;155:367–76.PubMed 

    Google Scholar 
    de Goeij JM, van Oevelen D, Vermiej MJA, Osinga R, Middelburg JJ, de Goeij AFPM, et al. Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science. 2013;342:108–10.PubMed 

    Google Scholar 
    de Goeij JM, Lesser MP, Pawlik JR. Nutrient fluxes and ecological functions of coral reef sponges in a changing ocean. In: Carballo, J, Bell, J eds. Climate Change, Ocean Acidification and Sponges. Springer, 2017. pp 373–410.Tanaka Y, Miyajima T, Wtanabe A, Nadaoka K, Yamamoto T, Ogawa H. Distribution of dissolved organic carbon and nitrogen in a coral reef. Coral Reefs. 2011;30:533–41.
    Google Scholar 
    Lesser MP, Slattery M, Laverick JH, Macartney KJ, Bridge TC. Global community breaks at 61 m on mesophotic coral reefs. Global Ecol Biogeogr. 2019;28:1403–16.
    Google Scholar 
    Lønborg C, Álvarez-Salgado XA, Duggan S, Carreira C. Organic matter bioavailability in tropical coastal waters: The Great Barrier Reef. Limnol Oceanogr. 2018;63:1015–35.
    Google Scholar 
    Macartney KJ, Abraham AC, Slattery M, Lesser MP. Growth and feeding in the sponge Agelas tubulata from shallow to mesophotic depths on Grand Cayman Island. Ecosphere. 2021;12:e03764.
    Google Scholar 
    Ribes M, Coma R, Atkinson MJ, Kinzie RA. Particle removal by coral reef communities: picoplankton is a major source of nitrogen. Mar Ecol Prog Ser. 2003;257:13–23.
    Google Scholar 
    Ribes M, Coma R, Atkinson MJ, Kinzie RA. Sponges and ascidians control removal of particulate organic nitrogen from coral reef water. Limnol Oceanogr. 2005;50:1480–9.CAS 

    Google Scholar 
    Maldonado M, Ribes M, van Duyl FC. Nutrient fluxes through sponges: biology, budgets, and ecological implications. Adv Mar Biol. 2012;62:113–82.PubMed 

    Google Scholar 
    Seutin G, White BN, Boag PT. Preservation of avian blood and tissue samples for DNA analyses. Can J Zool. 1991;69:82–90.CAS 

    Google Scholar 
    Abraham AC, Gochfeld DJ, Macartney K, Mellow A, Lesser MP, Slattery M. Biochemical variability in sponges across the Caribbean basin. Invertebr Biol. 2021;140:e12341.
    Google Scholar 
    Sunagawa S, Woodley CM, Medina M. Threatened corals provide underexplored microbial habitats. PLoS One. 2010;5:e9554.PubMed 
    PubMed Central 

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

    Google Scholar 
    Apprill A, McNally S, Parsons R, Weber L. Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquat Microb Ecol. 2015;75:129–37.
    Google Scholar 
    Simion P, Phillippe H, Baurain D, Jager M, Richter RJ, Di Franco A, et al. A Large and consistent phylogenomic dataset supports sponges as the sister group to all other animals. Curr Biol. 2017;27:958–67.CAS 
    PubMed 

    Google Scholar 
    Katoh K, Misawa K, Kuma KI, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30:3059–66.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Oksanen J, Simpson GL, Blanchet FG, Kindt R, Legendre P, Minchin PR, et al. vegan: Community Ecology Package. R package version 2.5-5. https://CRAN.R-project.org/package=vegan. Released May, 2019.Pinheiro J, Bates D, DebRoy S, Sarkar D, EISPACK Authors, Heisterkamp S, et al. nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-155. https://svn.r-project.org/R-packages/trunk/nlme/. Released Jan, 2022.Kindt R, Coe R. Tree diversity analysis. A manual and software for common statistical methods for ecological and biodiversity studies. World Agroforestry Centre, ICRAF, 2005. https://www.worldagroforestry.org/publication/tree-diversity-analysis-manual-and-software-common-statistical-methods-ecological-and.Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.PubMed 
    PubMed Central 

    Google Scholar 
    Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Westbrook A, Ramsdell J, Schuelke T, Normington L, Bergeron RD, Thomas WK, et al. PALADIN: protein alignment for functional profiling whole metagenome shotgun data. Bioinformatics. 2017;33:1473–8.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Robinson MD, McCarthy DG, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139–40.CAS 
    PubMed 

    Google Scholar 
    Li D, Luo R, Liu C-M, Leung C-M, Ting H-F, Sadakane K, et al. MEGAHIT v1.0: A fast and scalable metagenome assembler driven by advanced methodologies and community practices. Methods. 2016;102:3–11.CAS 
    PubMed 

    Google Scholar 
    Li H, Durbin R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics. 2009;25:1754–60.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Blin K, Shaw S, Kautsar SA, Medema MH, Weber T. The antiSMASH database version 3: increased taxonomic coverage and new query features for modular enzymes. Nucleic Acids Res. 2009;49:D639–43.
    Google Scholar 
    Conte-Jerpe IE, Thompson PD, Wong CWM, Oliveira NL, Duprey NN, Moynihan MA, et al. Trophic strategy and bleaching resistance in reef-building corals. Sci Adv. 2020;6:eaaz5443.
    Google Scholar 
    Jackson AL, Inger R, Parnell AC, Bearhop S. Comparing isotopic niche widths among and within communities: SIBER-Stable Isotope Bayesian Ellipses. Anim Ecol. 2011;80:595–602.
    Google Scholar 
    Thomas T, Moitinho-Silva L, Lurgi M, Björk JR, Easson C, Astudillo-Garcia C, et al. Diversity, structure and convergent evolution of the global sponge microbiome. Nat Comm. 2016;7:11870.CAS 

    Google Scholar 
    Erwin PM, Coma R, López-Sendino P, Serrano E, Ribes M. Stable symbionts across the HMA-LMA dichotomy: low seasonal and inter-annual variation in sponge-associated bacteria from taxonomically diverse hosts. FEMS Microbiol Ecol. 2015;91:fiv115.PubMed 

    Google Scholar 
    Moitinho-Silva L, Steinert G, Nielsen S, Hardoim CCP, Wu Y-C, McCormack GP. Predicting the HMA-LMA status in marine sponges by machine learning. Front Microbiol. 2017;8:752.PubMed 
    PubMed Central 

    Google Scholar 
    Campana S, Demey C, Busch K, Hentschel U, Muyzer G, de Goeij J. Marine sponges maintain stable bacterial communities between reef sites with different coral to algae cover ratios. FEMS Microbiol Ecol. 2021;97:fiab115.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Freeman CJ, Thacker RW. Complex interactions between marine sponges and their symbiotic microbial communities. Limnol Oceanogr. 2011;56:1577–86.
    Google Scholar 
    Siegel A, Kamke J, Hochmuth T, Piel J, Richter M, Liang C, et al. Single-cell genomic reveals the lifestyle of Poribacteria, a candidate phylum symbiotically associated with marine sponges. ISME J. 2011;5:61–70.
    Google Scholar 
    Bayer K, Jahn MT, Slaby BM, Moitinho-Silva L, Hentschel U. Marine sponges as Chloroflexi hot spots: genomic insights and high resolution visualization of an abundant and diverse symbiotic clade. mSystems. 2018;3:e00150–18.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Fan L, Reynolds D, Liu M, Thomas T. Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts. Proc Natl Acad Sci USA. 2012;109:1878–87.
    Google Scholar 
    Ribes M, Jiménez E, Yahel G, López-Sendino P, Diez B, Massana R, et al. Functional convergence of microbes associated with temperate marine sponges. Environ Microbiol. 2012;14:1224–39.CAS 
    PubMed 

    Google Scholar 
    Thomas T, Rusch D, DeMaere MZ, Yung PY, Lewis M, Halpern A, et al. Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis. ISME J. 2010;4:1557–67.CAS 
    PubMed 

    Google Scholar 
    Fiore CL, Labrie M, Jarett JK, Lesser MP. Transcriptional activity of the giant barrel sponge, Xestospongia muta holobiont: molecular evidence for metabolic interchange. Front Microbiol. 2015;6:364.PubMed 
    PubMed Central 

    Google Scholar 
    Engel S, Pawlik JR. Allelopathic activities of sponge extracts. Mar Ecol Prog Ser. 2000;207:273–82.
    Google Scholar 
    Gochfeld DJ, Kamel HN, Olson JB, Thacker RW. Trade-offs in defensive metabolite production but not ecological function in healthy and diseased sponges. J Chem Ecol. 2012;38:451–62.CAS 
    PubMed 

    Google Scholar 
    van Duyl FC, Mueller B, Meesters EH. Spatio-temporal variation in stable isotopic signatures (δ13C and δ15N) of sponges on the Saba Bank. PeerJ. 2018;6:e5460.PubMed 
    PubMed Central 

    Google Scholar 
    Fiore CL, Baker DM, Lesser MP. Nitrogen biogeochemistry in the Caribbean sponge, Xestospongia muta: a source or sink of dissolved inorganic nitrogen? PLoS One. 2013;8:e72961.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Hudspith M, de Goeij JM, Streekstra M, Kornder NA, Bougoure J, Guagliardo P, et al. Harnessing solar power: photoautotrophy supplements the diet of a low-light dwelling sponge. ISME J. 2022; https://doi.org/10.1038/s41396-022-01254-3.Shih JL, Selph KE, Wall CB, Wallsgrove NJ, Lesser MP, Popp BN. Trophic ecology of the tropical Pacific sponge Mycale gradis inferred from amino acid compound-specific isotopic analyses. Microb Ecol. 2020;79:495–510.CAS 
    PubMed 

    Google Scholar 
    Macartney KJ, Slattery M, Lesser MP. Trophic ecology of Caribbean sponges in the mesophotic zone. Limnol Oceanogr. 2021;66:1113–24.CAS 

    Google Scholar 
    Southwell MW, Popp BN, Martens CS. Nitrification controls on fluxes and isotopic composition of nitrate from Florida Keys sponges. Mar Chem. 2008;108:96–108.CAS 

    Google Scholar 
    Lamb K, Swart PK. The carbon and nitrogen isotopic values of particulate organic material from the Florida Keys: a temporal and spatial study. Coral Reefs. 2008;27:351–62.
    Google Scholar 
    Ferrier-Pagès C, Leal MG. Stable isotopes as tracers of trophic interactions in marine mutualistic symbioses. Ecol Evol. 2019;9:723–40.PubMed 

    Google Scholar 
    McMurray SE, Stubler AD, Erwin PM, Finelli CM, Pawlik JR. A test of the sponge-loop hypothesis for emergent Caribbean reef sponges. Mar Ecol Prog Ser. 2018;588:1–14.CAS 

    Google Scholar 
    Freeman CJ, Easson CG, Baker DM. Metabolic diversity and niche structure in sponges from the Miskito Cays, Honduras. PeerJ. 2014;2:e695.PubMed 
    PubMed Central 

    Google Scholar 
    Freeman CJ, Easson CG, Matterson KO, Thacker RW, Baker DM, Paul VJ. Microbial symbionts and ecological divergence of Caribbean sponges: a new perspective on an ancient association. ISME J. 2020;14:1571–83.PubMed 
    PubMed Central 

    Google Scholar 
    Poppell E, Weisz J, Spicer L, Massaro A, Hill A, Hill M. Sponge heterotrophic capacity and bacterial community structure in high‐and low‐microbial abundance sponges. Mar Ecol. 2014;35:414–24.
    Google Scholar 
    Morganti TM, Ribes M, Yahel G, Coma R. Size is the major determinant of pumping rates in marine sponges. Front Physiol. 2019;10:1474.PubMed 
    PubMed Central 

    Google Scholar 
    Rix L, Ribes M, Coma R, Jahn MT, de Goeij JM, van Oevelen D, et al. Heterotrophy in the earliest gut: a single-cell view of heterotrophic carbon and nitrogen assimilation in sponge-microbe symbioses. ISME J. 2020;14:2554–67.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    O’Brien PA, Tan S, Yang C, Frade PR, Andreakis N, Smith HA, et al. Diverse coral reef invertebrates exhibit patterns of phylosymbiosis. ISME J. 2020;14:2211–22.PubMed 
    PubMed Central 

    Google Scholar 
    Erwin PM, Thacker RW. Incidence and identity of photosynthetic symbionts in Caribbean coral reef sponge assemblages. J Mar Biol Assoc UK. 2007;87:1683–92.CAS 

    Google Scholar 
    Palumbi SR. Tactics of acclimation: morphological changes of sponges in an unpredictable environment. Science. 1984;225:1478–80.CAS 
    PubMed 

    Google Scholar 
    Slattery M, Gochfeld DJ, Diaz MC, Thacker RW, Lesser MP. Variability in chemical defense across a shallow to mesophotic depth gradient in the Caribbean sponge Plakortis angulospiculatus. Coral Reefs. 2016;35:11–22.
    Google Scholar 
    Morganti T, Coma R, Yahel G, Ribes M. Trophic niche separation that facilitates co‐existence of high and low microbial abundance sponges is revealed by in situ study of carbon and nitrogen fluxes. Limnol Oceanogr. 2017;62:1963–83.CAS 

    Google Scholar 
    Maldonado M. Sponge waste that fuels marine oligotrophic food webs: a re-assessment of its origin and nature. Mar Ecol. 2016;37:477–91.
    Google Scholar  More