More stories

  • in

    Transmission of stony coral tissue loss disease (SCTLD) in simulated ballast water confirms the potential for ship-born spread

    Precht, W. F., Gintert, B. E., Robbart, M. L., Fura, R. & van Woesik, R. Unprecedented disease-related coral mortality in Southeastern Florida. Sci. Rep. 6, 31374 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    NOAA. Stony Coral Tissue Loss Disease Case Definition. NOAA, Silver Spring, MD 10 (2018).Aeby, G. S. et al. Pathogenesis of a tissue loss disease affecting multiple species of corals along the Florida Reef Tract. Front Mar. Sci. 6, 00678 (2019).
    Google Scholar 
    Landsberg, J. H. et al. Stony coral tissue loss disease in Florida is associated with disruption of host–zooxanthellae physiology. Front Mar. Sci. 7, 576013 (2020).
    Google Scholar 
    Neely, K. L., Macaulay, K. A., Hower, E. K. & Dobler, M. A. Effectiveness of topical antibiotics in treating corals affected by Stony Coral Tissue Loss Disease. PeerJ 8, 9289 (2020).
    Google Scholar 
    Shilling, E. N., Combs, I. R. & Voss, J. D. Assessing the effectiveness of two intervention methods for stony coral tissue loss disease on Montastraea cavernosa. Sci. Rep. 11, 8566 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Walker, B. K., Turner, N. R., Noren, H. K. G., Buckley, S. F. & Pitts, K. A. Optimizing stony coral tissue loss disease (SCTLD) intervention treatments on Montastraea cavernosa in an endemic zone. Front Mar. Sci. 8, 666224 (2021).
    Google Scholar 
    Work, T. M. et al. Viral-like particles are associated with endosymbiont pathology in Florida corals affected by stony coral tissue loss disease. Front Mar. Sci. 8, 750658 (2021).
    Google Scholar 
    Veglia, A. J. et al. Alphaflexivirus genomes in stony coral tissue loss disease-affected, disease-exposed, and disease-unexposed coral colonies in the U.S. Virgin Islands. Microbiol. Resource Announc. 11, e01199-e1221 (2022).CAS 

    Google Scholar 
    Rosales, S. M. et al. Bacterial metabolic potential and micro-eukaryotes enriched in stony coral tissue loss disease lesions. Front Mar. Sci. 8, 776859 (2022).
    Google Scholar 
    Rosales, S. M., Clark, A. S., Huebner, L. K., Ruzicka, R. R. & Muller, E. M. Rhodobacterales and Rhizobiales are associated with stony coral tissue loss disease and its suspected sources of transmission. Front. Microbiol. 11, 681 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    Studivan, M. S. et al. Reef sediments can act as a stony coral tissue loss disease vector. Front Mar. Sci. 8, 815698 (2022).
    Google Scholar 
    Meyer, J. L. et al. Microbial community shifts associated with the ongoing stony coral tissue loss disease outbreak on the Florida Reef Tract. Front. Microbiol. 10, 2244 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    Ushijima, B. et al. Disease diagnostics and potential coinfections by Vibrio coralliilyticus during an ongoing coral disease outbreak in Florida. Front. Microbiol. 11, 2682 (2020).
    Google Scholar 
    Meiling, S. S. et al. Variable species responses to experimental stony coral tissue loss disease (SCTLD) exposure. Front Mar. Sci. 8, 670829 (2021).
    Google Scholar 
    Becker, C. C., Brandt, M., Miller, C. A. & Apprill, A. Microbial bioindicators of stony coral tissue loss disease identified in corals and overlying waters using a rapid field-based sequencing approach. Environ. Microbiol. 24, 1166–1182 (2021).PubMed 

    Google Scholar 
    Dobbelaere, T., Muller, E. M., Gramer, L. J., Holstein, D. M. & Hanert, E. Coupled epidemio-hydrodynamic modeling to understand the spread of a deadly coral disease in Florida. Front Mar. Sci. 7, 591881 (2020).
    Google Scholar 
    Dobbelaere, T. et al. Connecting the dots: Transmission of stony coral tissue loss disease from the Marquesas to the Dry Tortugas. Front Mar. Sci. 9, 778938 (2022).
    Google Scholar 
    Muller, E. M., Sartor, C., Alcaraz, N. I. & van Woesik, R. Spatial epidemiology of the stony-coral-tissue-loss disease in Florida. Front Mar. Sci. 7, 00163 (2020).
    Google Scholar 
    Sharp, W. C., Shea, C. P., Maxwell, K. E., Muller, E. M. & Hunt, J. H. Evaluating the small-scale epidemiology of the stony-coral-tissue-loss-disease in the middle Florida Keys. PLoS ONE 15, e0241871 (2020).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Williamson, O. M., Dennison, C. E., O’Neil, K. L. & Baker, A. C. Susceptibility of Caribbean brain coral recruits to stony coral tissue loss disease (SCTLD). Front Mar. Sci. 9, 821165 (2022).
    Google Scholar 
    Noonan, K. R. & Childress, M. J. Association of butterflyfishes and stony coral tissue loss disease in the Florida Keys. Coral Reefs 39, 1581–1590 (2020).
    Google Scholar 
    Dahlgren, C., Pizarro, V., Sherman, K., Greene, W. & Oliver, J. Spatial and temporal patterns of stony coral tissue loss disease outbreaks in the Bahamas. Front Mar. Sci. 8, 682114 (2021).
    Google Scholar 
    Rosenau, N. A. et al. Considering commercial vessels as potential vectors of stony coral tissue loss disease. Front Mar. Sci. 8, 709764 (2021).
    Google Scholar 
    Roth, L., Kramer, P., Doyle, E. & O’Sullivan, C. Caribbean SCTLD Dashboard. Available www.agrra.org. Accessed 06 Mar 2021. (2020).Brandt, M. E. et al. The emergence and initial impact of stony coral tissue loss disease (SCTLD) in the United States Virgin Islands. Front Mar. Sci. 8, 715329 (2021).
    Google Scholar 
    Bailey, S. A. et al. Trends in the detection of aquatic non-indigenous species across global marine, estuarine and freshwater ecosystems: A 50-year perspective. Divers. Distrib. 26, 1780–1797 (2020).MathSciNet 

    Google Scholar 
    Hewitt, C. L., Gollasch, S. & Minchin, D. The vessel as a vector: Biofouling, ballast water and sediments. In Biological Invasions in Marine Ecosystems Vol. 204 (eds Rilov, G. & Crooks, J. A.) 117–131 (Springer, 2009).
    Google Scholar 
    Zabin, C. J. et al. Small boats provide connectivity for nonindigenous marine species between a highly invaded international port and nearby coastal harbors. Manag. Biol. Invas. 5, 97–112 (2014).
    Google Scholar 
    Ashton, G. V., Zabin, C. J., Davidson, I. C. & Ruiz, G. M. Recreational boats routinely transfer organisms and promote marine bioinvasions. Biol. Invas. 24, 1083–1096 (2022).
    Google Scholar 
    Drake, L. A., Doblin, M. A. & Dobbs, F. C. Potential microbial bioinvasions via ships’ ballast water, sediment, and biofilm. Mar. Pollut. Bull. 55, 333–341 (2007).CAS 
    PubMed 

    Google Scholar 
    Pagenkopp Lohan, K. M., Fleischer, R. C., Carney, K. J., Holzer, K. K. & Ruiz, G. M. Amplicon-based pyrosequencing reveals high diversity of protistan parasites in ships’ ballast water: Implications for biogeography and infectious diseases. Microb. Ecol. 71, 530–542 (2015).PubMed 

    Google Scholar 
    Ruiz, G. M. et al. Global spread of microorganisms by ships. Nature 408, 49–50 (2000).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Hwang, J., Park, S. Y., Lee, S. & Lee, T. K. High diversity and potential translocation of DNA viruses in ballast water. Mar. Pollut. Bull. 137, 449–455 (2018).CAS 
    PubMed 

    Google Scholar 
    Shikuma, N. J. & Hadfield, M. G. Marine biofilms on submerged surfaces are a reservoir for Escherichia coli and Vibrio cholerae. Biofouling 26, 39–46 (2009).
    Google Scholar 
    Aguirre-Macedo, M. L. et al. Ballast water as a vector of coral pathogens in the Gulf of Mexico: The case of the Cayo Arcas coral reef. Mar. Pollut. Bull. 56, 1570–1577 (2008).CAS 
    PubMed 

    Google Scholar 
    Bruno, J. F. The coral disease triangle. Nat. Clim. Chang. 5, 302–303 (2015).ADS 

    Google Scholar 
    Lakshmi, E., Priya, M. & Achari, V. S. An overview on the treatment of ballast water in ships. Ocean Coast. Manag. 199, 105296 (2021).
    Google Scholar 
    Petersen, N. B., Madsen, T., Glaring, M. A., Dobbs, F. C. & Jørgensen, N. O. G. Ballast water treatment and bacteria: Analysis of bacterial activity and diversity after treatment of simulated ballast water by electrochlorination and UV exposure. Sci. Total Environ. 648, 408–421 (2019).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Romero-Martínez, L., Moreno-Andrés, J., Acevedo-Merino, A. & Nebot, E. Evaluation of ultraviolet disinfection of microalgae by growth modeling: Application to ballast water treatment. J. Appl. Phycol. 28, 2831–2842 (2016).
    Google Scholar 
    First, M. R. et al. Stratification of living organisms in ballast tanks: How do organism concentrations vary as ballast water is discharged?. Environ. Sci. Technol. 47, 4442–4448 (2013).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Drake, L. A. et al. Microbial ecology of ballast water during a transoceanic voyage and the effects of open-ocean exchange. Mar. Ecol. Prog. Ser. 233, 13–20 (2002).ADS 

    Google Scholar 
    Khandeparker, L., Kuchi, N., Desai, D. V. & Anil, A. C. Changes in the ballast water tank bacterial community during a trans-sea voyage: Elucidation through next generation DNA sequencing. J. Environ. Manag. 273, 111018 (2020).
    Google Scholar 
    Ruiz, G. M., Lorda, J., Arnwine, A. & Lion, K. Shipping patterns associated with the Panama Canal: Effects on biotic exchange? In Bridging Divides Vol. 83 (eds Gollasch, S. et al.) 113–126 (Springer, 2006).
    Google Scholar 
    Pagano, A., Wang, G., Sánchez, O., Ungo, R. & Tapiero, E. The impact of the Panama Canal expansion on Panama’s maritime cluster. Marit. Policy Manag. 43, 164–178 (2016).
    Google Scholar 
    Muirhead, J. R., Minton, M. S., Miller, W. A. & Ruiz, G. M. Projected effects of the Panama Canal expansion on shipping traffic and biological invasions. Divers. Distrib. 21, 75–87 (2015).
    Google Scholar 
    Ros, M. et al. The Panama Canal and the transoceanic dispersal of marine invertebrates: Evaluation of the introduced amphipod Paracaprella pusilla Mayer, 1890 in the Pacific Ocean. Mar. Environ. Res. 99, 204–211 (2014).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Stehouwer, P. P., Buma, A. & Peperzak, L. A comparison of six different ballast water treatment systems based on UV radiation, electrochlorination and chlorine dioxide. Environ. Technol. 36, 2094–2104 (2015).CAS 
    PubMed 

    Google Scholar 
    Wu, Y., Li, Z., Du, W. & Gao, K. Physiological response of marine centric diatoms to ultraviolet radiation, with special reference to cell size. J. Photochem. Photobiol., B 153, 1–6 (2015).CAS 

    Google Scholar 
    Aguirre, L. E. et al. Diatom frustules protect DNA from ultraviolet light. Sci. Rep. 8, 5138 (2018).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    First, M. R. & Drake, L. A. Life after treatment: Detecting living microorganisms following exposure to UV light and chlorine dioxide. J. Appl. Phycol. 26, 227–235 (2014).CAS 

    Google Scholar 
    Liebich, V., Stehouwer, P. P. & Veldhuis, M. Re-growth of potential invasive phytoplankton following UV-based ballast water treatment. Aquat. Invas. 7, 29–36 (2012).
    Google Scholar 
    Hess-Erga, O. K., Moreno-Andrés, J., Enger, Ø. & Vadstein, O. Microorganisms in ballast water: Disinfection, community dynamics, and implications for management. Sci. Total Environ. 657, 704–716 (2019).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Endresen, Ø., Lee Behrens, H., Brynestad, S., Bjørn Andersen, A. & Skjong, R. Challenges in global ballast water management. Mar. Pollut. Bull. 48, 615–623 (2004).CAS 
    PubMed 

    Google Scholar 
    Vorkapić, A., Radonja, R. & Zec, D. Cost efficiency of ballast water treatment systems based on ultraviolet irradiation and electrochlorination. Promet Traffic Transp. 30, 343–348 (2018).
    Google Scholar 
    King, D., Hagan, P., Riggio, M. & Wright, D. Preview of global ballast water treatment markets. J. Mar. Eng. Technol. 11, 3–15 (2012).
    Google Scholar 
    Wang, Z., Saebi, M., Corbett, J. J., Grey, E. K. & Curasi, S. R. Integrated biological risk and cost model analysis supports a geopolitical shift in ballast water management. Environ. Sci. Technol. 55, 12791–12800 (2021).CAS 
    PubMed 

    Google Scholar 
    Moreno-Andrés, J. & Peperzak, L. Operational and environmental factors affecting disinfection byproducts formation in ballast water treatment systems. Chemosphere 232, 496–505 (2019).ADS 
    PubMed 

    Google Scholar 
    David, M., Linders, J., Gollasch, S. & David, J. Is the aquatic environment sufficiently protected from chemicals discharged with treated ballast water from vessels worldwide? A decadal environmental perspective and risk assessment. Chemosphere 207, 590–600 (2018).ADS 
    CAS 
    PubMed 

    Google Scholar 
    U.S. Environmental Protection Agency. Generic protocol for the verification of ballast water treatment technology, version 5.1. Report number EPA/600/R-10/146. Washington, D.C. 157 (2010).Evans, J. S., Paul, V. J., Ushijima, B. & Kellogg, C. A. Combining tangential flow filtration and size fractionation of mesocosm water as a method for the investigation of waterborne coral diseases. Biol. Methods Protocols 7, bpac007 (2022).
    Google Scholar 
    Fujimoto, M. et al. Application of Ion Torrent sequencing to the assessment of the effect of alkali ballast water treatment on microbial community diversity. PLoS ONE 9, e107534 (2014).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    United States Coast Guard. Ballast Water Best Management Practices to Reduce the Likelihood of Transporting Pathogens That May Spread Stony Coral Tissue Loss Disease. Marine Safety Information Bulletin 07–19. Washington, D.C. 2 (2019).Bolton, J. R. & Linden, K. G. Standardization of methods for fluence (UV dose) determination in bench-scale UV experiments. J. Environ. Eng. 129, 209–215 (2003).CAS 

    Google Scholar 
    Enochs, I. C. et al. The influence of diel carbonate chemistry fluctuations on the calcification rate of Acropora cervicornis under present day and future acidification conditions. J. Exp. Mar. Biol. Ecol. 506, 135–143 (2018).CAS 

    Google Scholar 
    R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/. Preprint at https://www.r-project.org/ (2019).Therneau, T. M. survival: A package for survival analysis in R. R package version 3.2–13. (2021).Kassambara, A., Kosinski, M. & Biecek, P. survminer: Drawing survival curves using “ggplot2”. R package version 0.4.9. (2021).Bakalar, G. Review of interdisciplinary devices for detecting the quality of ship ballast water. Springerplus 3, 468 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    Water Environmental Federation & American Public Health Association. Standard methods for the examination of water and wastewater. Washington, D.C. 21 (2005).Steinberg, M. K., Lemieux, E. J. & Drake, L. A. Determining the viability of marine protists using a combination of vital, fluorescent stains. Mar. Biol. 158, 1431–1437 (2011).
    Google Scholar 
    Oksanen, J. et al. vegan: Community ecology package. R package version 2.0–10. (2015).Martinez Arbizu, P. pairwiseAdonis: Pairwise multilevel comparison using adonis. R package version 0.4. (2020).Studivan, MS. Mstudiva/SCTLD-ballast-transmission: Stony coral tissue loss disease ballast transmission and treatment (Version 1.0), Zenodo, https://doi.org/10.5281/zenodo.6561517 (2022). More

  • in

    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

    African perspectives on climate change research

    Urbanization is fast progressing in the Global South, requiring new solutions for infrastructure, services, industrial development and land and energy use for these regions. In this context, fast-growing cities in Africa can take on a leadership role in driving climate change mitigation and adaptation, disaster risk reduction and sustainable development.
    Credit: Stefan Rotter / Alamy Stock PhotoCities in Africa and elsewhere in the Global South continue to grapple with the challenge of delivering equitable services, infrastructure, housing and action to respond to climate change extremes and disasters. One well-known problem is a mismatch between the pace of urban growth and the slower development of basic services and critical infrastructure. This results in, for example, deficient sanitation, water supply systems and localized waste management for large parts of the population, which in turn contribute substantially to heightened poverty and inequality. For inclusive, equitable, prosperous and climate-resilient cities, urban management needs to integrate low-income communities into the urban economy by ensuring access to water, sanitation, energy transition, waste management, poverty reduction and by improving resilience through innovative solutions.
    Credit: Patrick J. Endres/Corbis Documentary/GettySuch an equitable urban transition requires changes in the urban infrastructure, and land and energy use, as well as water and ecosystem management. The key research question in this field is to find ways to ensure city-wide access to infrastructure and services, while minimizing emissions and resource use, and building resilience to climate change impacts. In this regard, cities in the Global South and Africa in particular can serve as examples for other parts of the world as they have the potential to adopt disruptive, innovative yet practical solutions to low emissions, resource minimization and resilience building.
    Credit: Nature Picture Library / Alamy Stock PhotoFor example, rapid urbanization creates the opportunity to develop economic structures in African cities that strongly integrate waste by promoting recovery, recycling, re-use and repair for lengthening lifecycles. Such a circular economy can create business opportunities, while also reducing resource use, thus creating a pathway for sustainable development. Another potential solution is hybrid systems for urban water management that are off-grid and utilize multiple water sources and treatment but that can also connect to centralized water systems. Business models for micro-to-medium enterprises have the potential to integrate some of the low-income groups through these kinds of technology and building social resilience.
    Credit: Images of Africa Photobank / Alamy Stock PhotoThese examples are part of a broader assessment of urban infrastructure innovations, their disruption of centralized systems and rethinking of urban form for more compact, walkable, co-located land use for low carbon intensity towards net-zero cities. However, to translate research on these new solutions into action, a shift is necessary in the planning, governing and managing of cities so as to allow for opportunities for leapfrogging to emerge and expand the possibilities of urban development for inclusive and resilient African cities. 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

    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

  • in

    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

  • 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

  • in

    Nitrogen-fixing symbiotic bacteria act as a global filter for plant establishment on islands

    Delavaux, C. S., Smith‐Ramesh, L. M. & Kuebbing, S. E. Beyond nutrients: a meta‐analysis of the diverse effects of arbuscular mycorrhizal fungi on plants and soils. Ecology 98, 2111–2119 (2017).Lugtenberg, B. & Kamilova, F. Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63, 541–556 (2009).Article 
    CAS 
    PubMed 

    Google Scholar 
    Franche, C., Lindström, K. & Elmerich, C. Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil 321, 35–59 (2009).Article 
    CAS 

    Google Scholar 
    Razanajatovo, M. et al. Autofertility and self‐compatibility moderately benefit island colonization of plants. Glob. Ecol. Biogeogr. 28, 341–352 (2019).Article 

    Google Scholar 
    Schrader, J., Wright, I. J., Kreft, H. & Westoby, M. A roadmap to plant functional island biogeography. Biol. Rev. (2021).Herridge, D. F., Peoples, M. B. & Boddey, R. M. Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 311, 1–18 (2008).Article 
    CAS 

    Google Scholar 
    Vitousek, P. Nutrient cycling and limitation: Hawai’i as a model ecosystem. (Princeton Univ. Press, Princeton, NJ, 2004). Nutrient cycling and limitation: Hawai’i as a model ecosystem. Princeton Univ. Press, Princeton, NJ.Book 

    Google Scholar 
    Becking, L. G. M. B. Geobiologie of inleiding tot de milieukunde. (WP Van Stockum & Zoon, 1934).Peay, K. G. & Bruns, T. D. Spore dispersal of basidiomycete fungi at the landscape scale is driven by stochastic and deterministic processes and generates variability in plant–fungal interactions. N. Phytol. 204, 180–191 (2014).Article 

    Google Scholar 
    Delavaux, C. S. et al. Mycorrhizal fungi influence global plant biogeography. Nat. Ecol. Evol. 3, 424 (2019).Article 
    PubMed 

    Google Scholar 
    Duchicela, J., Bever, J. D. & Schultz, P. A. Symbionts as Filters of Plant Colonization of Islands: Tests of Expected Patterns and Environmental Consequences in the Galapagos. Plants 9, 74 (2020).Article 
    CAS 
    PubMed Central 

    Google Scholar 
    Delavaux, C. S. et al. Mycorrhizal types influence island biogeography of plants. Commun. Biol. 4, 1–8 (2021).Article 

    Google Scholar 
    Simonsen, A. K., Dinnage, R., Barrett, L. G., Prober, S. M. & Thrall, P. H. Symbiosis limits establishment of legumes outside their native range at a global scale. Nat. Commun. 8, 1–9 (2017).Article 

    Google Scholar 
    Poole, P., Ramachandran, V. & Terpolilli, J. Rhizobia: from saprophytes to endosymbionts. Nat. Rev. Microbiol. 16, 291–303 (2018).Article 
    CAS 
    PubMed 

    Google Scholar 
    Sprent, J. I., Ardley, J. & James, E. K. Biogeography of nodulated legumes and their nitrogen‐fixing symbionts. N. Phytol. 215, 40–56 (2017).Article 
    CAS 

    Google Scholar 
    Menge, D. N. Hedin, L. O. & Pacala, S. W. Nitrogen and phosphorus limitation over long-term ecosystem development in terrestrial ecosystems. (2012).Lambers, H., Raven, J. A., Shaver, G. R. & Smith, S. E. Plant nutrient-acquisition strategies change with soil age. Trends Ecol. evolution 23, 95–103 (2008).Article 

    Google Scholar 
    Walker, T. & Syers, J. K. The fate of phosphorus during pedogenesis. Geoderma 15, 1–19 (1976).Article 
    CAS 

    Google Scholar 
    Jin, L. et al. Synergistic interactions of arbuscular mycorrhizal fungi and rhizobia promoted the growth of Lathyrus sativus under sulphate salt stress. Symbiosis 50, 157–164 (2010).Article 
    CAS 

    Google Scholar 
    Afkhami, M. E. & Stinchcombe, J. R. Multiple mutualist effects on genomewide expression in the tripartite association between Medicago truncatula, nitrogen‐fixing bacteria and mycorrhizal fungi. Mol. Ecol. 25, 4946–4962 (2016).Article 
    CAS 
    PubMed 

    Google Scholar 
    Larimer, A. L., Clay, K. & Bever, J. D. Synergism and context dependency of interactions between arbuscular mycorrhizal fungi and rhizobia with a prairie legume. Ecology 95, 1045–1054 (2014).Article 
    PubMed 

    Google Scholar 
    Primieri, S., Magnoli, S. M., Koffel, T. S., Stürmer, S. L. & Bever, J. D. Perennial, but not annual legumes synergistically benefit from infection with arbuscular mycorrhizal fungi and rhizobia: a meta‐analysis. N. Phytol. 233, 505-514 (2021).Larimer, A. L., Bever, J. D. & Clay, K. The interactive effects of plant microbial symbionts: a review and meta-analysis. Symbiosis 51, 139–148 (2010).Article 

    Google Scholar 
    Werner, G. D., Cornwell, W. K., Sprent, J. I., Kattge, J. & Kiers, E. T. A single evolutionary innovation drives the deep evolution of symbiotic N 2-fixation in angiosperms. Nat. Commun. 5, 1–9 (2014).Article 

    Google Scholar 
    Weigelt, P., König, C. & Kreft, H. GIFT- A global inventory of floras and traits for macroecology and biogeography. J. Biogeogr. 47, 16–43 (2020).Article 

    Google Scholar 
    Werner, G. D. et al. Symbiont switching and alternative resource acquisition strategies drive mutualism breakdown. Proc. Natl Acad. Sci. 115, 5229–5234 (2018).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bamba, M. et al. Wide distribution range of rhizobial symbionts associated with pantropical sea-dispersed legumes. Antonie van. Leeuwenhoek 109, 1605–1614 (2016).Article 
    PubMed 

    Google Scholar 
    Chen, W.-M., Lee, T.-M., Lan, C.-C. & Cheng, C.-P. Characterization of halotolerant rhizobia isolated from root nodules of Canavalia rosea from seaside areas. FEMS Microbiol. Ecol. 34, 9–16 (2000).Article 
    CAS 
    PubMed 

    Google Scholar 
    Toma, M. A. et al. Tripartite symbiosis of Sophora tomentosa, rhizobia and arbuscular mycorhizal fungi. Braz. J. Microbiol. 48, 680–688 (2017).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Elanchezhian, R., Rajalakshmi, S. & Jayakumar, V. Salt tolerance characteristics of rhizobium species associated with Vigna marina. Indian J. Agric. Sci. 79, 980–985 (2009).CAS 

    Google Scholar 
    Chapin, F. S., Matson, P. A., Mooney, H. A. & Vitousek, P. M. Principles of Terrestrial Ecosystem Ecology (Springer, 2002).Vitousek, P. M., Walker, L. R., Whiteaker, L. D. & Matson, P. A. Nutrient limitations to plant growth during primary succession in Hawaii Volcanoes National Park. Biogeochemistry 23, 197–215 (1993).Article 

    Google Scholar 
    Liao, C. et al. Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis. N. Phytologist 177, 706–714 (2008).Article 
    CAS 

    Google Scholar 
    Woodward, S. A. et al. Use of the Exotic Tree Myrica Faya by Native and Exotic Birds in Hawai’i Volcanoes National Park (University of Hawaii Press, 1990).Vitousek, P. M., Walker, L. R., Whiteaker, L. D., Mueller-Dombois, D. & Matson, P. A. Biological invasion by Myrica faya alters ecosystem development in Hawaii. Science 238, 802–804 (1987).Article 
    CAS 
    PubMed 

    Google Scholar 
    Theoharides, K. A. & Dukes, J. S. Plant invasion across space and time: factors affecting nonindigenous species success during four stages of invasion. N. phytologist 176, 256–273 (2007).Article 

    Google Scholar 
    Kalwij, J. M. Review of ‘The Plant List, a working list of all plant species’. J. Vegetation Sci. 23, 998–1002 (2012).Article 

    Google Scholar 
    Byng, J. W. et al. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical J. Linn. Soc. 181, 1–20 (2016).Article 

    Google Scholar 
    Soudzilovskaia, N. A. et al. FungalRoot: Global online database of plant mycorrhizal associations. N. Phytol. 227, 955–966 (2020).Article 

    Google Scholar 
    Weigelt, P., König, C. & Kreft, H. GIFT–A global inventory of floras and traits for macroecology and biogeography. J. Biogeogr. 47, 16–43 (2020).Article 

    Google Scholar 
    Karger, D. N. et al. Climatologies at high resolution for the earth’s land surface areas. Sci. Data 4, 170122 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Danielson, J. J. & Gesch, D. B. “Global multi-resolution terrain elevation data 2010 (GMTED2010),” (US Geological Survey, 2011).Weigelt, P. & Kreft, H. Quantifying island isolation–insights from global patterns of insular plant species richness. Ecography 36, 417–429 (2013).Article 

    Google Scholar 
    Kreft, H., Jetz, W., Mutke, J., Kier, G. & Barthlott, W. Global diversity of island floras from a macroecological perspective. Ecol. Lett. 11, 116–127 (2008).PubMed 

    Google Scholar 
    Triantis, K. A., Economo, E. P., Guilhaumon, F. & Ricklefs, R. E. Diversity regulation at macro‐scales: species richness on oceanic archipelagos. Glob. Ecol. Biogeogr. 24, 594–605 (2015).Article 

    Google Scholar 
    Crase, B., Liedloff, A. C. & Wintle, B. A. A new method for dealing with residual spatial autocorrelation in species distribution models. Ecography 35, 879–888 (2012).Article 

    Google Scholar 
    Bivand, R. R packages for analyzing spatial data: a comparative case study with areal data. Geogr. Anal. 54, 488–518 (2022).Article 

    Google Scholar 
    R. C. Team, R: A language and environment for statistical computing. (R Foundation for Statistical Computing, 2019).Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting Linear Mixed-Effects Models Using lme4. J. Stat. Softw. 67, 1–48 (2015).Article 

    Google Scholar  More