More stories

  • in

    Mapping marine debris encountered by albatrosses tracked over oceanic waters

    1.Cózar, A. et al. Plastic debris in the open ocean. Proc. Nat. Acad. Sci. USA 111, 10239–10244. https://doi.org/10.1073/pnas.1314705111 (2014).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    2.Lavers, J. L., Dicks, L., Dicks, M. R. & Finger, A. Significant plastic accumulation on the Cocos (Keeling) Islands, Australia. Sci. Rep. 9, 7102. https://doi.org/10.1038/s41598-019-43375-4 (2019).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    3.Cózar, A. et al. The arctic ocean as a dead end for floating plastics in the north atlantic branch of the thermohaline circulation. Sci. Adv. https://doi.org/10.1126/sciadv.1600582 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    4.Peeken, I. et al. Arctic sea ice is an important temporal sink and means of transport for microplastic. Nat. Commun. 9, 1505. https://doi.org/10.1038/s41467-018-03825-5 (2018).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    5.Woodall, L. C. et al. The deep sea is a major sink for microplastic debris. R. Soc. Open Sci. 1, 140317 (2014).ADS 
    Article 

    Google Scholar 
    6.Chiba, S. et al. Human footprint in the abyss: 30 year records of deep-sea plastic debris. Mar. Policy 96, 204–212. https://doi.org/10.1016/j.marpol.2018.03.022 (2018).Article 

    Google Scholar 
    7.Bergmann, M., Tekman, M. & Gutow, L. Sea change for plastic pollution. Nature 544, 297 (2017).ADS 
    CAS 
    Article 

    Google Scholar 
    8.Jambeck, J. R. et al. Plastic waste inputs from land into the ocean. Science 347, 768–771. https://doi.org/10.1126/science.1260352 (2015).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    9.Gall, S. C. & Thompson, R. C. The impact of debris on marine life. Mar. Pollut. Bull. 92, 170–179. https://doi.org/10.1016/j.marpolbul.2014.12.041 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    10.Camphuysen, C. J. Northern Gannets Morus bassanus found dead in the Netherlands, 1970–2000. Atlantic Seabirds 3, 15–30 (2001).
    Google Scholar 
    11.Gregory, M. R. Environmental implications of plastic debris in marine settings–entanglement, ingestion, smothering, hangers-on, hitch-hiking and alien invasions. Phil. Trans. R. Soc. B 364, 2013–2025 (2009).Article 

    Google Scholar 
    12.Ryan, P. G. The effects of ingested plastic on seabirds: Correlations between plastic load and body condition. Environ. Pollut. 46, 119–125 (1987).CAS 
    Article 

    Google Scholar 
    13.Ryan, P. G. Effects of ingested plastic on seabird feeding: Evidence from chickens. Mar. Pollut. Bull. 19, 125–128 (1988).Article 

    Google Scholar 
    14.Pierce, K. E., Harris, R. J., Larned, L. S. & Pokras, M. A. Obstruction and starvation associated with plastic ingestion in a Northern Gannet Morus bassanus and a greater shearwater Puffinus gravis. Mar. Ornithol. 32, 187–189 (2004).
    Google Scholar 
    15.Ryan, P. G., Connell, A. D. & Gardner, B. D. Plastic ingestion and PCBs in seabirds: Is there a relationship?. Mar. Pollut. Bull. 19, 174–176 (1988).CAS 
    Article 

    Google Scholar 
    16.Lavers, J. L., Bond, A. L. & Hutton, I. Plastic ingestion by Flesh-footed Shearwaters (Puffinus carneipes): Implications for chick body condition and the accumulation of plastic-derived chemicals. Environ. Pollut. 187, 124–129. https://doi.org/10.1016/j.envpol.2013.12.020 (2014).CAS 
    Article 
    PubMed 

    Google Scholar 
    17.Tanaka, K. et al. In vivo accumulation of plastic-derived chemicals into seabird tissues. Curr. Biol. 30, 723-728.e3. https://doi.org/10.1016/j.cub.2019.12.037 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    18.Teuten, E. L. et al. Transport and release of chemicals from plastics to the environment and to wildlife. Phil. Trans. R. Soc. B 364, 2027–2045 (2009).CAS 
    Article 

    Google Scholar 
    19.Tanaka, K., van Franeker, J. A., Deguchi, T. & Takada, H. Piece-by-piece analysis of additives and manufacturing byproducts in plastics ingested by seabirds: Implication for risk of exposure to seabirds. Mar. Pollut. Bull. 145, 36–41. https://doi.org/10.1016/j.marpolbul.2019.05.028 (2019).CAS 
    Article 
    PubMed 

    Google Scholar 
    20.Thiel, M. & Gutow, L. The ecology of rafting in the marine environment. I. The floating substrata. Oceanogr. Mar. Biol. Annu. Rev. 42, 181–264 (2005).
    Google Scholar 
    21.Kiessling, T., Gutow, L. & Thiel, M. Marine litter as habitat and dispersal vector. In: Bergmann M, Gutow L, Klages M, editors. Marine Anthropogenic Litter. p. 141–80 (2015).22.Day, R. H. & Shaw, D. G. Patterns of abundance of pelagic plastic and tar in the North Pacific Ocean, 1976–1985. Mar. Pollut. Bull. 18, 311–316 (1987).CAS 
    Article 

    Google Scholar 
    23.Pichel, W. G. et al. Marine debris collects within the North Pacific Subtropical Convergence Zone. Mar. Pollut. Bull. 54, 1207–1211 (2007).CAS 
    Article 

    Google Scholar 
    24.Yamashita, R. & Tanimura, A. Floating plastic in the Kuroshio Current area, western North Pacific Ocean. Mar. Pollut. Bull. 54, 485–488 (2007).CAS 
    Article 

    Google Scholar 
    25.Titmus, A. J. & Hyrenbach, K. D. Habitat associations of floating debris and marine birds in the North East Pacific Ocean at coarse and meso spatial scales. Mar. Pollut. Bull. 62, 2496–2506 (2011).CAS 
    Article 

    Google Scholar 
    26.Goldstein, M. C., Titmus, A. J. & Ford, M. Scales of spatial heterogeneity of plastic marine debris in the northeast pacific ocean. PLoS ONE 8, e80020 (2013).ADS 
    Article 

    Google Scholar 
    27.Eriksen, M. et al. Plastic pollution in the world’s oceans: More than 5 trillion plastic pieces weighing over 250,000 tons afloat at sea. PLoS ONE 9, e111913 (2014).ADS 
    Article 

    Google Scholar 
    28.IUCN. The IUCN Red List of Threatened Species. Version 2020–2. https://www.iucnredlist.org (2020).29.Lavers, J. L. & Bond, A. L. Ingested plastic as a route for trace metals in Laysan Albatross (Phoebastria immutabilis) and Bonin Petrel (Pterodroma hypoleuca) from Midway Atoll. Mar. Pollut. Bull. 110, 493–500. https://doi.org/10.1016/j.marpolbul.2016.06.001 (2016).CAS 
    Article 
    PubMed 

    Google Scholar 
    30.Roman, L., Hardesty, B. D., Hindell, M. A. & Wilcox, C. A quantitative analysis linking seabird mortality and marine debris ingestion. Sci. Rep. 9, 3202. https://doi.org/10.1038/s41598-018-36585-9 (2019).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    31.Jouventin, P. & Weimerskirch, H. Satellite tracking of wandering albatrosses. Nature 343, 746–748 (1990).ADS 
    Article 

    Google Scholar 
    32.Kappes, M. A. et al. Hawaiian albatrosses track interannual variability of marine habitats in the North Pacific. Prog. Oceanogr. 86, 246–260 (2010).ADS 
    Article 

    Google Scholar 
    33.Sakamoto, K. Q., Takahashi, A., Iwata, T. & Trathan, P. N. From the eye of the albatrosses: A bird-borne camera shows an association between albatrosses and a killer whale in the Southern Ocean. PLoS ONE 4, e7322 (2009).ADS 
    Article 

    Google Scholar 
    34.Fukuoka, T. et al. The feeding habit of sea turtles influences their reaction to artificial marine debris. Sci. Rep. 6, 28015. https://doi.org/10.1038/srep28015 (2016).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    35.Nishizawa, B. et al. Albatross-borne loggers show feeding on deep-sea squids: Implications for the study of squid distributions. Mar. Ecol. Prog. Ser. 592, 257–265 (2018).ADS 
    Article 

    Google Scholar 
    36.Hunt, G. L. Jr. & Schneider, D. Scale-dependent processes in the physical and biological environment of marine birds. In Seabirds: Feeding Ecology and Role in Marine Ecosystems (ed. Croxall, J. P.) 7–41 (Cambridge University Press, 1987).
    Google Scholar 
    37.Pinaud, D. & Weimerskirch, H. At-sea distribution and scale-dependent foraging behaviour of petrels and albatrosses: A comparative study. J. Anim. Ecol. 76, 9–19 (2007).Article 

    Google Scholar 
    38.Thiebot, J.-B., Nishizawa, B., Sato, F., Tomita, N. & Watanuki, Y. Albatross chicks reveal interactions of adults with artisanal longline fisheries within a short range. J. Ornithol. 159, 935–944 (2018).Article 

    Google Scholar 
    39.Froese, R. & Pauly, D. FishBase. World Wide Web electronic publication. www.fishbase.org, version (12/2019).40.Ryan, P. G. A simple technique for counting marine debris at sea reveals steep litter gradients between the Straits of Malacca and the Bay of Bengal. Mar. Pollut. Bull. 69, 128–136 (2013).CAS 
    Article 

    Google Scholar 
    41.Mitani, Y. et al. Marine debris observed in the North Pacific during Oshoro-maru cruise in 2012. Bull. Fish. Sci. Hokkaido Univ. 64, 25–29 (2014).
    Google Scholar 
    42.Hyrenbach, K. D. et al. Plastic ingestion by Black-footed albatross from Kure Atoll, Hawai’i: linking chick loads and parental at-sea distributions. Mar. Ornithol. 45, 225–236 (2017).
    Google Scholar 
    43.Nevitt, G. A., Losekoot, M. & Weimerskirch, H. Evidence for olfactory search in wandering albatross, Diomedea Exulans. Proc. Nat. Acad. Sci. USA 105, 4576–4581 (2008).ADS 
    CAS 
    Article 

    Google Scholar 
    44.Savoca, M. S., Wohlfeil, M. E., Ebeler, S. E. & Nevitt, G. A. Marine plastic debris emits a keystone infochemical for olfactory foraging seabirds. Sci. Adv. 2, e1600395 (2016).ADS 
    Article 

    Google Scholar 
    45.Santos, R. G., Andrades, R., Fardim, L. M. & Martins, A. S. Marine debris ingestion and Thayer’s law—The importance of plastic color. Environ. Pollut. 214, 585–588 (2016).CAS 
    Article 

    Google Scholar 
    46.Castro, J. J., Santiago, J. A. & Santana-Ortega, A. T. A general theory on fish aggregation to floating objects: An alternative to the meeting point hypothesis. Rev. Fish Biol. Fish. 11, 255–277 (2002).Article 

    Google Scholar 
    47.Harrison, C. S., Hida, T. S. & Seki, M. P. Hawaiian seabird feeding ecology. Wildl. Monogr. 85, 1–71 (1983).
    Google Scholar 
    48.Hunte, W., Oxenford, H. A. & Mahon, R. Distribution and relative abundance of flyingfish (Exocoetidae) in the eastern Caribbean. II. Spawning substrata, eggs and larvae. Mar. Ecol. Prog. Ser. 117, 25–37 (1995).ADS 
    Article 

    Google Scholar 
    49.Rapp, D. C., Youngren, S. M., Hartzell, P. & Hyrenbach, K. D. Community-wide patterns of plastic ingestion in seabirds breeding at French Frigate Shoals Northwestern Hawaiian Islands. Mar. Pollut. Bull. 123, 269–278 (2017).CAS 
    Article 

    Google Scholar 
    50.Douglas, D. & Peucker, T. Algorithms for the reduction of the number of points required to represent a digitized line or its caricature. Cannadian Cartogr. 10, 112–122 (1973).Article 

    Google Scholar 
    51.Edelhoff, H., Signer, J. & Balkenhol, N. Path segmentation for beginners: an overview of current methods for detecting changes in animal movement patterns. Move. Ecol. 4, 21 (2016).Article 

    Google Scholar 
    52.R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.r-project.org/index.html (2020). More

  • in

    Variable coastal hypoxia exposure and drivers across the southern California Current

    1.Díaz, R. J. Overview of hypoxia around the world. J. Environ. Qual. 30, 275–281 (2001).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    2.Laffoley, D. & Baxter, J. M. (eds) Ocean deoxygenation: Everyone’s problem. Causes, impacts, consequences and solutions (IUCN, International Union for Conservation of Nature, 2019).
    Google Scholar 
    3.Booth, J. A. T. et al. Patterns and potential drivers of declining oxygen content along the southern California coast. Limnol. Oceanogr. 59, 1127–1138 (2014).ADS 
    CAS 
    Article 

    Google Scholar 
    4.Gilbert, D., Rabalais, N. N., Díaz, R. J. & Zhang, J. Evidence for greater oxygen decline rates in the coastal ocean than in the open ocean. Biogeosciences 7, 2283–2296 (2010).ADS 
    CAS 
    Article 

    Google Scholar 
    5.Altieri, A. H. & Gedan, K. B. Climate change and dead zones. Glob. Change Biol. 21, 1395–1406 (2015).ADS 
    Article 

    Google Scholar 
    6.Breitburg, D. et al. Declining oxygen in the global ocean and coastal waters. Science (80-) 359, eaam7240 (2018).Article 
    CAS 

    Google Scholar 
    7.Keeling, R. E., Körtzinger, A. & Gruber, N. Ocean deoxygenation in a warming world. Ann. Rev. Mar. Sci. 2, 199–229 (2010).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    8.Levin, L. A. & Breitburg, D. L. Linking coasts and seas to address ocean deoxygenation. Nat. Clim. Change 5, 401–403 (2015).ADS 
    Article 

    Google Scholar 
    9.Rabalais, N. N., Turner, R. E., Díaz, R. J. & Justić, D. Global change and eutrophication of coastal waters. ICES J. Mar. Sci. 66, 1528–1537 (2009).Article 

    Google Scholar 
    10.Diaz, R. J. & Rosenberg, R. Spreading dead zones and consequences for marine ecosystems. Science (80-) 321, 926–929 (2008).ADS 
    CAS 
    Article 

    Google Scholar 
    11.Hofmann, A. F., Peltzer, E. T., Walz, P. M. & Brewer, P. G. Hypoxia by degrees: Establishing definitions for a changing ocean. Deep Res. Part I Oceanogr. Res. Pap. 58, 1212–1226 (2011).ADS 
    CAS 
    Article 

    Google Scholar 
    12.Rabalais, N. N. et al. Dynamics and distribution of natural and human-caused hypoxia. Biogeosciences 7, 585–619 (2010).ADS 
    CAS 
    Article 

    Google Scholar 
    13.Vaquer-Sunyer, R. & Duarte, C. M. Thresholds of hypoxia for marine biodiversity. Proc. Natl. Acad. Sci. 105, 15452–15457 (2008).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    14.Altieri, A. H. et al. Tropical dead zones and mass mortalities on coral reefs. Proc. Natl. Acad. Sci. U. S. A. 114, 3660–3665 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    15.Grantham, B. A. et al. Upwelling-driven nearshore hypoxia signals ecosystem and oceanographic changes in the northeast Pacific. Nature 429, 749–754 (2004).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    16.Kim, T. W., Barry, J. P. & Micheli, F. The effects of intermittent exposure to low-pH and low-oxygen conditions on survival and growth of juvenile red abalone. Biogeosciences 10, 7255–7262 (2013).ADS 
    Article 

    Google Scholar 
    17.Kolesar, S. E., Breitburg, D. L., Purcell, J. E. & Decker, M. B. Effects of hypoxia on Mnemiopsis leidyi, ichthyoplankton and copepods: Clearance rates and vertical habitat overlap. Mar. Ecol. Prog. Ser. 411, 173–188 (2010).ADS 
    CAS 
    Article 

    Google Scholar 
    18.Low, N. H. N. & Micheli, F. Lethal and functional thresholds of hypoxia in two key benthic grazers. Mar. Ecol. Prog. Ser. 594, 165–173 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    19.Thomas, P. & Saydur Rahman, M. Extensive reproductive disruption, ovarian masculinization and aromatase suppression in Atlantic croaker in the northern Gulf of Mexico hypoxic zone. Proc. R. Soc. B Biol. Sci. 279, 28–38 (2011).Article 
    CAS 

    Google Scholar 
    20.Breitburg, D. Effects of hypoxia, and the balance between hypoxia and enrichment, on coastal fishes and fisheries. Estuaries 25, 767–781 (2002).Article 

    Google Scholar 
    21.Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).Article 

    Google Scholar 
    22.Pörtner, H. O. & Knust, R. Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science (80-) 315, 95–97 (2007).ADS 
    Article 
    CAS 

    Google Scholar 
    23.Vaquer-Sunyer, R. & Duarte, C. M. Temperature effects on oxygen thresholds for hypoxia in marine benthic organisms. Glob. Change Biol. 17, 1788–1797 (2011).ADS 
    Article 

    Google Scholar 
    24.Breitburg, D. L., Hondorp, D. W., Davias, L. A. & Diaz, R. J. Hypoxia, nitrogen, and fisheries: Integrating effects across local and global landscapes. Ann. Rev. Mar. Sci. 1, 329–349 (2009).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    25.Booth, J. A. T. et al. Natural intrusions of hypoxic, low pH water into nearshore marine environments on the California coast. Cont. Shelf. Res. 45, 108–115 (2012).ADS 
    Article 

    Google Scholar 
    26.Walter, R. K., Woodson, C. B., Leary, P. R. & Monismith, S. G. Connecting wind-driven upwelling and offshore stratification to nearshore internal bores and oxygen variability. J. Geophys. Res. Ocean 119, 3517–3534 (2014).ADS 
    Article 

    Google Scholar 
    27.Boch, C. A. et al. Local oceanographic variability influences the performance of juvenile abalone under climate change. Sci. Rep. 8, 1–12 (2018).CAS 
    Article 

    Google Scholar 
    28.DiMarco, S. F., Chapman, P., Walker, N. & Hetland, R. D. Does local topography control hypoxia on the eastern Texas–Louisiana shelf?. J. Mar. Syst. 80, 25–35 (2010).Article 

    Google Scholar 
    29.Leary, P. R. et al. “Internal tide pools” prolong kelp forest hypoxic events. Limnol. Oceanogr. 62, 2864–2878 (2017).ADS 
    CAS 
    Article 

    Google Scholar 
    30.Walter, R. K., Brock Woodson, C., Arthur, R. S., Fringer, O. B. & Monismith, S. G. Nearshore internal bores and turbulent mixing in southern Monterey Bay. J. Geophys. Res. Ocean 117, 1–13 (2012).
    Google Scholar 
    31.Long, W. C. & Seitz, R. D. Trophic interactions under stress: Hypoxia enhances foraging in an estuarine food web. Mar. Ecol. Prog. Ser. 362, 59–68 (2008).ADS 
    Article 

    Google Scholar 
    32.Kwiatkowski, L. & Orr, J. C. Diverging seasonal extremes for ocean acidification during the twenty-first centuryr. Nat. Clim. Chang. 8, 141–145 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    33.Safaie, A. et al. High frequency temperature variability reduces the risk of coral bleaching. Nat. Commun. 9, 1–12 (2018).Article 
    CAS 

    Google Scholar 
    34.Woodson, C. B. The fate and impact of internal waves in nearshore ecosystems. Ann. Rev. Mar. Sci. 10, 421–441 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    35.Woodson, C. B. et al. Harnessing marine microclimates for climate change adaptation and marine conservation. Conserv. Lett. 12(2), 1–9 (2018).
    Google Scholar 
    36.Micheli, F. et al. Evidence that marine reserves enhance resilience to climatic impacts. PLoS ONE 7, e40832 (2012).
    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    37.Cox, K. W. California abalones, family haliotidae. Fish. Bull. 118 28–32 (1962).

    Google Scholar 
    38.Frieder, C. A., Nam, S. H., Martz, T. R. & Levin, L. A. High temporal and spatial variability of dissolved oxygen and pH in a nearshore California kelp forest. Biogeosciences 9, 3917–3930 (2012).ADS 
    CAS 
    Article 

    Google Scholar 
    39.Mayol, E., Ruiz-Halpern, S., Duarte, C. M., Castilla, J. C. & Pelegrí, J. L. Coupled CO2 and O2-driven compromises to marine life in summer along the Chilean sector of the Humboldt Current System. Biogeosciences 9, 1183–1194 (2012).ADS 
    CAS 
    Article 

    Google Scholar 
    40.Orellana-Cepeda, E., Granados-Machuca, C. & Serrano-Esquer, J. Ceratium furca: One possible cause of mass mortality of cultured Blue-Fin Tuna at Baja California, Mexico. Harmful Algae 2002, 514–516 (2004).
    Google Scholar 
    41.Bograd, S. J. et al. Oxygen declines and the shoaling of the hypoxic boundary in the California Current. Geophys. Res. Lett. 35, 1–6 (2008).Article 
    CAS 

    Google Scholar 
    42.Bernardi, G., Findley, L. & Rocha-Olivares, A. Vicariance and dispersal across Baja California in disjunct marine fish populations. Evolution (N Y) 57, 1599–1609 (2003).
    Google Scholar 
    43.Haupt, A. J., Micheli, F. & Palumbi, S. R. Dispersal at a snail’s pace: Historical processes affect contemporary genetic structure in the exploited wavy top snail (Megastraea undosa). J. Hered. 104, 327–340 (2013).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    44.Al Najjar, M. W. Nearshore Processes of a Coastal Island: Physical Dynamics and Ecological Implications (Stanford University, 2019).
    Google Scholar 
    45.Hughes, B. B. et al. Climate mediates hypoxic stress on fish diversity and nursery function at the land-sea interface. Proc. Natl. Acad. Sci. U. S. A. 112, 8025–8030 (2015).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    46.Sydeman, W. J. et al. Climate change and wind intensification in coastal upwelling ecosystems. Science (80-) 345, 77–80 (2014).ADS 
    CAS 
    Article 

    Google Scholar 
    47.Fulton, S. et al. From fishing fish to fishing data: The role of Artisanal Fishers in Conservation and Resource Management in Mexico. In Viability and Sustainability of Small-Scale Fisheries in Latin America and The Caribbean (eds Salas, S. et al.) 151–175 (Springer International Publishing, 2019).
    Google Scholar 
    48.Chang, W., Cheng, J., Allaire, J. J., Xie, Y. & McPherson, J. shiny: Web Application Framework for R. R package version 1.4.0.2. https://cran.r-project.org/package=shiny (2020).49.R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (2020).50.Eerkes-Medrano, D., Menge, B. A., Sislak, C. & Langdon, C. J. Contrasting effects of hypoxic conditions on survivorship of planktonic larvae of rocky intertidal invertebrates. Mar. Ecol. Prog. Ser. 478, 139–151 (2013).ADS 
    Article 

    Google Scholar 
    51.Low, N. H. N. & Micheli, F. Short- and long-term impacts of variable hypoxia exposures on kelp forest sea urchins. Sci. Rep. 10, 1–9 (2020).CAS 
    Article 

    Google Scholar 
    52.Bograd, S. J. et al. Phenology of coastal upwelling in the California Current. Geophys. Res. Lett. 36, 1–5 (2009).Article 

    Google Scholar 
    53.Nam, S., Kim, H. J. & Send, U. Amplification of hypoxic and acidic events by la Nia conditions on the continental shelf off California. Geophys. Res. Lett. 38, 1–5 (2011).Article 
    CAS 

    Google Scholar 
    54.Rogers-Bennett, L. et al. Dinoflagellate bloom coincides with marine invertebrate mortalities in Northern California. Harmful Algae News 46, 10–11 (2012).
    Google Scholar 
    55.Chan, F. et al. Persistent spatial structuring of coastal ocean acidification in the California Current System. Sci. Rep. 7, 1–8 (2017).Article 
    CAS 

    Google Scholar 
    56.Montgomery, D. W., Simpson, S. D., Engelhard, G. H., Birchenough, S. N. R. & Wilson, R. W. Rising CO2 enhances hypoxia tolerance in a marine fish. Sci. Rep. 9, 1–10 (2019).CAS 
    Article 

    Google Scholar 
    57.Boch, C. A. et al. Effects of current and future coastal upwelling conditions on the fertilization success of the red abalone (Haliotis rufescens). ICES J. Mar. Sci. 74, 1125–1134 (2017).Article 

    Google Scholar 
    58.Gobler, C. J. & Baumann, H. Hypoxia and acidification in marine ecosystems: Coupled dynamics and effects on
    ocean life. Biol. Lett. 12, 20150976 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar  More

  • in

    Arbuscular mycorrhizal trees influence the latitudinal beta-diversity gradient of tree communities in forests worldwide

    1.Myers, J. A. & LaManna, J. A. The promise and pitfalls of beta-diversity in ecology and conservation. J. Veg. Sci. 27, 1081–1083 (2016).Article 

    Google Scholar 
    2.Socolar, J. B., Gilroy, J. J., Kunin, W. E. & Edwards, D. P. How should beta-diversity inform biodiversity conservation? Trends Ecol. Evol. 31, 67–80 (2016).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    3.Xing, D. L. & He, F. L. Environmental filtering explains a U-shape latitudinal pattern in regional beta-deviation for eastern North American trees. Ecol. Lett. 22, 284–291 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    4.Anderson, M. J. et al. Navigating the multiple meanings of beta diversity: a roadmap for the practicing ecologist. Ecol. Lett. 14, 19–28 (2011).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    5.Baselga, A. Partitioning the turnover and nestedness components of beta diversity. Glob. Ecol. Biogeogr. 19, 134–143 (2010).Article 

    Google Scholar 
    6.Menegotto, A., Dambros, C. S. & Netto, S. A. The scale-dependent effect of environmental filters on species turnover and nestedness in an estuarine benthic community. Ecology 100, e02721 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    7.Whittaker, R. H. Vegetation of the Siskiyou mountains, Oregon and California. Ecol. Monogr. 30, 279–338 (1960).Article 

    Google Scholar 
    8.Hubbell, S. P. The unified neutral theory of biodiversity and biogeography. (Princeton University Press, 2001).9.Nekola, J. C. & White, P. S. The distance decay of similarity in biogeography and ecology. J. Biogeogr. 26, 867–878 (1999).Article 

    Google Scholar 
    10.da Silva, P. G., Lobo, J. M., Hensen, M. C., Vaz-de-Mello, F. Z. & Hernandez, M. I. M. Turnover and nestedness in subtropical dung beetle assemblages along an elevational gradient. Divers Distrib. 24, 1277–1290 (2018).Article 

    Google Scholar 
    11.Wang, X. G. et al. Ecological drivers of spatial community dissimilarity, species replacement and species nestedness across temperate forests. Glob. Ecol. Biogeogr. 27, 581–592 (2018).Article 

    Google Scholar 
    12.McFadden, I. R. et al. Temperature shapes opposing latitudinal gradients of plant taxonomic and phylogenetic beta diversity. Ecol. Lett. 22, 1126–1135 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    13.Qian, H., Chen, S., Mao, L. & Ouyang, Z. Drivers of β‐diversity along latitudinal gradients revisited. Glob. Ecol. Biogeogr. 22, 659–670 (2013).Article 

    Google Scholar 
    14.Xu, W. B., Chen, G. K., Liu, C. R. & Ma, K. P. Latitudinal differences in species abundance distributions, rather than spatial aggregation, explain beta-diversity along latitudinal gradients. Glob. Ecol. Biogeogr. 24, 1170–1180 (2015).Article 

    Google Scholar 
    15.Kraft, N. J. et al. Disentangling the drivers of β diversity along latitudinal and elevational gradients. Science 333, 1755–1758 (2011).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    16.Griffiths, D. Connectivity and vagility determine beta diversity and nestedness in North American and European freshwater fish. J. Biogeogr. 44, 1723–1733 (2017).Article 

    Google Scholar 
    17.Soininen, J., Heino, J. & Wang, J. J. A meta-analysis of nestedness and turnover components of beta diversity across organisms and ecosystems. Glob. Ecol. Biogeogr. 27, 96–109 (2018).Article 

    Google Scholar 
    18.LaManna, J. A., Belote, R. T., Burkle, L. A., Catano, C. P. & Myers, J. A. Negative density dependence mediates biodiversity-productivity relationships across scales. Nat. Ecol. Evol. 1, 1107–1115 (2017).PubMed 
    Article 
    PubMed Central 

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

    Google Scholar 
    20.Brundrett, M. C. Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320, 37–77 (2009).CAS 
    Article 

    Google Scholar 
    21.Gibert, A., Tozer, W. & Westoby, M. Plant performance response to eight different types of symbiosis. New Phytol. 222, 526–542 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    22.Veresoglou, S. D., Rillig, M. C. & Johnson, D. Responsiveness of plants to mycorrhiza regulates coexistence. J. Ecol. 106, 1864–1875 (2018).Article 

    Google Scholar 
    23.Delavaux, C. S. et al. Mycorrhizal fungi influence global plant biogeography. Nat. Ecol. Evol. 3, 424–429 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    24.Barcelo, M., van Bodegom, P. M. & Soudzilovskaia, N. A. Climate drives the spatial distribution of mycorrhizal host plants in terrestrial ecosystems. J. Ecol. 107, 2564–2573 (2019).Article 

    Google Scholar 
    25.Steidinger, B. S. et al. Climatic controls of decomposition drive the global biogeography of forest-tree symbioses. Nature 571, E8–E8 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    26.Bennett, J. A. et al. Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science 355, 181–184 (2017).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    27.Johnson, D. J., Clay, K. & Phillips, R. P. Mycorrhizal associations and the spatial structure of an old-growth forest community. Oecologia 186, 195–204 (2018).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    28.Hargreaves, A. L., Germain, R. M., Bontrager, M., Persi, J. & Angert, A. L. Local adaptation to biotic interactions: a meta-analysis across latitudes. Am. Nat. 195, 395–411 (2020).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    29.Liu, X. B. et al. Partitioning of soil phosphorus among arbuscular and ectomycorrhizal trees in tropical and subtropical forests. Ecol. Lett. 21, 713–723 (2018).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    30.Jacquemyn, H., De Kort, H., Vanden Broeck, A. & Brys, R. Immigrant and extrinsic hybrid seed inviability contribute to reproductive isolation between forest and dune ecotypes of Epipactis helleborine (Orchidaceae). Oikos 127, 73–84 (2018).Article 

    Google Scholar 
    31.Osborne, O. G. et al. Arbuscular mycorrhizal fungi promote coexistence and niche divergence of sympatric palm species on a remote oceanic island. New Phytol. 217, 1254–1266 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    32.Myers, J. A. et al. Beta-diversity in temperate and tropical forests reflects dissimilar mechanisms of community assembly. Ecol. Lett. 16, 151–157 (2013).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    33.Jankowski, J. E., Ciecka, A. L., Meyer, N. Y. & Rabenold, K. N. Beta diversity along environmental gradients: implications of habitat specialization in tropical montane landscapes. J. Anim. Ecol. 78, 315–327 (2009).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    34.McCarthy-Neumann, S. & Ibáñez, I. Tree range expansion may be enhanced by escape from negative plant–soil feedbacks. Ecology 93, 2637–2649 (2012).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    35.Peay, K. G. The mutualistic niche: mycorrhizal symbiosis and community dynamics. Annu. Rev. Ecol., Evol. Syst. 47, 143–164 (2016).Article 

    Google Scholar 
    36.Wang, Z. H., Fang, J. Y., Tang, Z. Y. & Shi, L. Geographical patterns in the beta diversity of China’s woody plants: the influence of space, environment and range size. Ecography 35, 1092–1102 (2012).Article 

    Google Scholar 
    37.Liang, M. X. et al. Soil fungal networks maintain local dominance of ectomycorrhizal trees. Nat. Commun. 11, 2636 (2020).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    38.Segnitz, R. M., Russo, S. E., Davies, S. J. & Peay, K. G. Ectomycorrhizal fungi drive positive phylogenetic plant-soil feedbacks in a regionally dominant tropical plant family. Ecology 101, e03083 (2020).39.Chen, L. et al. Differential soil fungus accumulation and density dependence of trees in a subtropical forest. Science 366, 124–128 (2019).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    40.Brundrett, Mark, Murase, Gracia & K, B. Comparative anatomy of roots and mycorrhizae of common Ontario trees. Can. J. Bot. 68, 551–578 (1990).Article 

    Google Scholar 
    41.Liu, Y. & He, F. L. Incorporating the disease triangle framework for testing the effect of soil-borne pathogens on tree species diversity. Funct. Ecol. 33, 1211–1222 (2019).MathSciNet 
    Article 

    Google Scholar 
    42.LaManna, J. A. et al. Plant diversity increases with the strength of negative density dependence at the global scale. Science 356, 1389–1392 (2017).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    43.Johnson, D. J., Beaulieu, W. T., Bever, J. D. & Clay, K. Conspecific negative density dependence and forest diversity. Science 336, 904–907 (2012).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    44.Crawford, K. M. et al. When and where plant-soil feedback may promote plant coexistence: a meta-analysis. Ecol. Lett. 22, 1274–1284 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    45.Liu, X. B., Etienne, R. S., Liang, M. X., Wang, Y. F. & Yu, S. X. Experimental evidence for an intraspecific Janzen-Connell effect mediated by soil biota. Ecology 96, 662–671 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    46.Chu, C. J. et al. Direct and indirect effects of climate on richness drive the latitudinal diversity gradient in forest trees. Ecol. Lett. 22, 245–255 (2019).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    47.Gavito, M. E. & Azcon-Aguilar, C. Temperature stress in arbuscular mycorrhizal fungi: a test for adaptation to soil temperature in three isolates of Funneliformis mosseae from different climates. Agr. Food Sci. 21, 2–11 (2012).Article 

    Google Scholar 
    48.Hetrick, B. D. & Bloom, J. The influence of temperature on colonization of winter wheat by vesicular-arbuscular mycorrhizal fungi. Mycologia 76, 953–956 (1984).Article 

    Google Scholar 
    49.Anderson-Teixeira, K. J. et al. CTFS-ForestGEO: a worldwide network monitoring forests in an era of global change. Glob. Change Biol. 21, 528–549 (2015).ADS 
    Article 

    Google Scholar 
    50.Condit, R. Tropical forest census plots: methods and results from Barro Colorado Island, Panama and a comparison with other plots. (Springer-Verlag andRG. Landes Company, 1998).51.Stillhard, J. et al. Stand inventory data from the 10-ha forest research plot in Uholka: 15 yr of primeval beech forest development. Ecology 100, e02845 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    52.Marion, Z. H., Fordyce, J. A. & Fitzpatrick, B. M. Pairwise beta diversity resolves an underappreciated source of confusion in calculating species turnover. Ecology 98, 933–939 (2017).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    53.Bennett, J. R. & Gilbert, B. Contrasting beta diversity among regions: how do classical and multivariate approaches compare? Glob. Ecol. Biogeogr. 25, 368–377 (2016).Article 

    Google Scholar 
    54.Legendre, P. & De Caceres, M. Beta diversity as the variance of community data: dissimilarity coefficients and partitioning. Ecol. Lett. 16, 951–963 (2013).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    55.Baselga, A. Separating the two components of abundance-based dissimilarity: balanced changes in abundance vs. abundance gradients. Methods Ecol. Evol. 4, 552–557 (2013).Article 

    Google Scholar 
    56.De Cáceres, M. et al. The variation of tree beta diversity across a global network of forest plots. Glob. Ecol. Biogeogr. 21, 1191–1202 (2012).Article 

    Google Scholar 
    57.Yen, J. D. L., Fleishman, E., Fogarty, F. & Dobkin, D. S. Relating beta diversity of birds and butterflies in the Great Basin to spatial resolution, environmental variables and trait-based groups. Glob. Ecol. Biogeogr. 28, 328–340 (2019).Article 

    Google Scholar 
    58.Craven, D., Knight, T. M., Barton, K. E., Bialic-Murphy, L. & Chase, J. M. Dissecting macroecological and macroevolutionary patterns of forest biodiversity across the Hawaiian archipelago. Proc. Natl Acad. Sci. USA 116, 16436–16441 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    59.Brundrett, M. & Tedersoo, L. Misdiagnosis of mycorrhizas and inappropriate recycling of data can lead to false conclusions. New Phytol. 221, 18–24 (2019).PubMed 
    Article 
    PubMed Central 

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

    Google Scholar 
    61.Furniss, T. J., Larson, A. J. & Lutz, J. A. Reconciling niches and neutrality in a subalpine temperate forest. Ecosphere 8 (2017).62.Jucker, T. et al. Canopy structure and topography jointly constrain the microclimate of human-modified tropical landscapes. Glob. Change Biol. 24, 5243–5258 (2018).ADS 
    Article 

    Google Scholar 
    63.Legendre, P. et al. Partitioning beta diversity in a subtropical broad-leaved forest of China. Ecology 90, 663–674 (2009).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    64.Robert J., H. raster: Geographic data analysis and modeling. R package version 2.6-7 (2017). .65.Alahuhta, J. et al. Global variation in the beta diversity of lake macrophytes is driven by environmental heterogeneity rather than latitude. J. Biogeogr. 44, 1758–1769 (2017).Article 

    Google Scholar 
    66.Cribari-Neto, F. & Zeileis, A. Beta regression in R. J. Stat. Softw. 34, 1–24 (2010).Article 

    Google Scholar 
    67.Jump, A. S., Matyas, C. & Penuelas, J. The altitude-for-latitude disparity in the range retractions of woody species. Trends Ecol. Evol. 24, 694–701 (2009).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    68.Oksanen, J. et al. vegan: Community ecology package. R package version 2.5-2 (2018). .69.Gilbert, B. & Bennett, J. R. Partitioning variation in ecological communities: do the numbers add up? J. Appl Ecol. 47, 1071–1082 (2010).Article 

    Google Scholar 
    70.Breiman, L. Random forests. Mach. Learn. 45, 5–32 (2001).MATH 
    Article 

    Google Scholar 
    71.R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria (2019). .72.Baselga, A., Orme, D., Villeger, S., De Bortoli, J. & Leprieur, F. Partitioning beta diversity into turnover and nestedness components. R package version 1.5.0 (2019). .73.Harrell Jr, F. E. & Dupont, C. Hmisc: Harrell miscellaneous. R package version 4.2-3 (2019). .74.Liaw, A. & Wiener, M. Classification and regression by randomForest. R News. 2, 18–22 (2002).
    Google Scholar 
    75.Archer, E. rfPermute: estimate permutation p-values for random forest importance metrics. R package version 2.1.6 (2018). . More

  • in

    Impact of diesel and biodiesel contamination on soil microbial community activity and structure

    1.Mnif, I., Sahnoun, R. & Ellouz-Chaabouni, S. Application of bacterial biosurfactants for enhanced removal and biodegradation of diesel oil. Process Saf. Environ. Prot. 109, 72–81 (2017).CAS 
    Article 

    Google Scholar 
    2.Abioye, O. P. Biological remediation of hydrocarbon and heavy metals contaminated soil. In Soil Contamination (ed. Pascucci, S.) 127–142 (InTech Europe, 2011).
    Google Scholar 
    3.Zarinkamar, F., Reypour, F. & Soleimanpour, S. Effect of diesel fuel contaminated soil on the germination and the growth of Festuca arundinacea. Res. J. Chem. Environ. Sci. 1, 37–41 (2013).
    Google Scholar 
    4.Ashnani, M. H. M., Johari, A., Hashim, H. & Hasani, E. A source of renewable energy in Malaysia, why biodiesel? Renew. Sustain. Energy Rev. 35, 244–257 (2014).Article 

    Google Scholar 
    5.Bücker, F. et al. Impact of biodiesel on biodeterioration of stored Brazilian diesel oil. Int. Biodeterior. Biodegrad. 65, 172–178 (2011).Article 
    CAS 

    Google Scholar 
    6.Hawrot-Paw, M. & Izwikow, M. Ecotoxicologial effects of biodiesel in the soil. J. Ecol. Eng. 16, 34–39 (2015).Article 

    Google Scholar 
    7.Restrepo-Flórez, J.-M., Bassi, A., Rehmann, L. & Thompson, M. R. Effect of biodiesel addition on microbial community structure in a simulated fuel storage system. Bioresour. Technol. 147, 456–463 (2013).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    8.Silva, G. S. et al. Biodegradability of soy biodiesel in microcosm experiments using soil from the Atlantic Rain Forest. Appl. Soil Ecol. 55, 27–35 (2012).Article 

    Google Scholar 
    9.Prosser, J. I. Dispersing misconceptions and identifying opportunities for the use of ‘omics’ in soil microbial ecology. Nat. Rev. Microbiol. 13, 439–446 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    10.Hawrot-Paw, M. & Martynus, M. The influence of diesel fuel and biodiesel on soil microbial biomass. Pol. J. Environ. Stud. 20, 497–501 (2011).CAS 

    Google Scholar 
    11.Lahel, A. et al. Effect of process parameters on the bioremediation of diesel contaminated soil by mixed microbial consortia. Int. Biodeterior. Biodegrad. 113, 375 (2016).CAS 
    Article 

    Google Scholar 
    12.Nwankwegu, A. S., Orji, M. U. & Onwosi, C. O. Studies on organic and in-organic biostimulants in bioremediation of diesel-contaminated arable soil. Chemosphere 162, 148–156 (2016).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    13.Woźniak-Karczewska, M. et al. Effect of bioaugmentation on long-term biodegradation of diesel/biodiesel blends in soil microcosms. Sci. Total Environ. 671, 948–958 (2019).ADS 
    Article 
    CAS 

    Google Scholar 
    14.Caspi, R. et al. The MetaCyc database of metabolic pathways and enzymes. Nucleic Acids Res. 46, D633–D639 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    15.Lapinskiene, A., Martinkus, P. & Rebzdaite, V. Eco-toxicological studies of diesel and biodiesel fuels in aerated soil. Environ. Pollut. 142, 432–437 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    16.Schiewer, S. & Horel, A. Biodiesel addition influences biodegradation rates of fresh and artificially weathered diesel fuel in Alaskan sand. J. Cold Reg. Eng. 31, 1–14 (2017).Article 

    Google Scholar 
    17.Schreier, C. G., Walker, W. J., Burns, J. & Wilkenfeld, R. Total organic carbon as a screening method for petroleum hydrocarbons. Chemosphere 39, 503–510 (1999).ADS 
    CAS 
    Article 

    Google Scholar 
    18.Nimmo, M. Carbon. In Encyclopedia of Analytical Science (eds Worsfold, P. & Alan Townshend, C. P.) 453–457 (Elsevier, 2005).
    Google Scholar 
    19.Margesin, R. & Schinner, F. Bioremediation of diesel-oil-contaminated alpine soils at low temperatures. Appl. Microbiol. Biotechnol. 47, 462–468 (1997).CAS 
    Article 

    Google Scholar 
    20.Møller, J., Winther, P., Lund, B., Kirkebjerg, K. & Westermann, P. Bioventing of diesel oil-contaminated soil: Comparison of degradation rates in soil based on actual oil concentration and on respirometric data. J. Ind. Microbiol. 16, 110–116 (1996).Article 

    Google Scholar 
    21.Nakatsu, C. H. Microbial processes: Community analysis. Ref. Modul. Earth Syst. Environ. Sci. https://doi.org/10.1016/B978-0-12-409548-9.05218-0 (2013).Article 

    Google Scholar 
    22.Margesin, R., Hämmerle, M. & Tscherko, D. Microbial activity and community composition during bioremediation of diesel-oil-contaminated soil: Effects of hydrocarbon concentration, fertilizers, and incubation time. Microb. Ecol. 53, 259–269 (2007).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    23.Owsianiak, M. et al. Biodegradation of diesel/biodiesel blends by a consortium of hydrocarbon degraders: Effect of the type of blend and the addition of biosurfactants. Bioresour. Technol. 100, 1497–1500 (2009).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    24.Quideau, S. A. et al. Extraction and analysis of microbial phospholipid fatty acids in soils. J. Vis. Exp. https://doi.org/10.3791/54360 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    25.Frostegård, Å., Tunlid, A. & Bååth, E. Use and misuse of PLFA measurements in soils. Soil Biol. Biochem. 43, 1–5 (2010).
    Google Scholar 
    26.Ruess, L. & Chamberlain, P. M. The fat that matters: Soil food web analysis using fatty acids and their carbon stable isotope signature. Soil Biol. Biochem. 42, 1898–1910 (2010).CAS 
    Article 

    Google Scholar 
    27.Davila, S. et al. Actinobacteria: Current research and perspectives for bioremediation of pesticides and heavy metals. Chemosphere 166, 41–62 (2017).ADS 
    Article 
    CAS 

    Google Scholar 
    28.Sutton, N. B. et al. Impact of long-term diesel contamination on soil microbial cummunity structure. Appl. Environ. Microbiol. 79, 619–630 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    29.Kersters, K., Vos, P. D. E., Gillis, M., Swings, J. & Vandamme, P. Introduction to the Proteobacteria. In The Prokaryotes: A Handbook on the Biology of Bacteria (eds Dworkin, M. et al.) 3–37 (Springer, 2006).
    Google Scholar 
    30.Bell, T. H. et al. Predictable bacterial composition and hydrocarbon degradation in Arctic soils following diesel and nutrient disturbance. ISME J. 7, 1200–1210 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    31.Brzeszcz, J. & Kaszycki, P. Aerobic bacteria degrading both n-alkanes and aromatic hydrocarbons: An undervalued strategy for metabolic diversity and flexibility. Biodegradation 29, 359–407 (2018).PubMed 
    Article 

    Google Scholar 
    32.Elumalai, P. et al. Role of thermophilic bacteria (Bacillus and, Geobacillus) on crude oil degradation and biocorrosion in oil reservoir environment. 3Biotech 9, 79 (2019).
    Google Scholar 
    33.Mitter, E. K., de Freitas, J. R. & Germida, J. J. Bacterial root microbiome of plants growing in oil sands reclamation covers. Front. Microbiol. https://doi.org/10.3389/fmicb.2017.00849 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    34.Bundy, J. G., Paton, G. I. & Campbell, C. D. Microbial communities in different soil types do not converge after diesel contamination. J. Appl. Microbiol. 92, 276–288 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    35.Korenblum, E., Souza, D. B., Penna, M. & Seldin, L. Molecular analysis of the bacterial communities in crude oil Samples from two Brazilian offshore petroleum platforms. Int. J. Microbiol. 2012, 1–8 (2012).Article 
    CAS 

    Google Scholar 
    36.Kim, T. J., Lee, E. Y., Kim, Y. J., Cho, K. S. & Ryu, H. W. Degradation of polyaromatic hydrocarbons by Burkholderia cepacia 2A–12. World J. Microbiol. Biotechnol. 19, 411–417 (2003).CAS 
    Article 

    Google Scholar 
    37.Revathy, T., Jayasri, M. A. & Suthindhiran, K. Biodegradation of PAHs by Burkholderia sp. VITRSB1 isolated from marine sediments. Scientifica (Cairo) 2015, 1–9 (2015).
    Google Scholar 
    38.Ramos, D. T., da Silva, M. L. B., Nossa, C. W., Alvarez, P. J. J. & Corseuil, H. X. Assessment of microbial communities associated with fermentative-methanogenic biodegradation of aromatic hydrocarbons in groundwater contaminated with a biodiesel blend (B20). Biodegradation 25, 681–691 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    39.Whyte, L. G. et al. Gene cloning and characterization of multiple alkane hydroxylase systems in Rhodococcus strains Q15 and NRRL B-16531. Appl. Environ. Microbiol. 68, 5933–5942 (2002).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    40.Lee, M., Kim, M. K., Singleton, I., Goodfellow, M. & Lee, S.-T. Enhanced biodegradation of diesel oil by a newly identified Rhodococcus baikonurensis EN3 in the presence of mycolic acid. J. Appl. Microbiol. 100, 325–333 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    41.Bateman, J. N., Speer, B., Feduik, L. & Hartline, R. A. Naphthalene association and uptake in Pseudomonas putida. J. Bacteriol. 166, 155–161 (1986).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    42.Rentz, J. A., Alvarez, P. J. J. & Schnoor, J. L. Repression of Pseudomonas putida phenanthrene-degrading activity by plant root extracts and exudates. Environ. Microbiol. 6, 574–583 (2004).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    43.Shukor, M. Y. et al. Isolation and characterization of Pseudomonas diesel-degrading strain from Antartica. J. Environ. Biol. 30, 1–6 (2009).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    44.Meyer, D. D. et al. Bioremediation strategies for diesel and biodiesel in oxisol from southern Brazil. Int. Biodeterior. Biodegrad. 95, 356–363 (2014).CAS 
    Article 

    Google Scholar 
    45.Taccari, M., Milanovic, V., Comitini, F., Casucci, C. & Ciani, M. Effects of biostimulation and bioaugmentation on diesel removal and bacterial community. Int. Biodeterior. Biodegrad. 66, 39–46 (2012).CAS 
    Article 

    Google Scholar 
    46.Fosso-Kankeu, E. et al. Adaptation behaviour of bacterial species and impact on the biodegradation of biodiesel-diesel. Braz. J. Chem. Eng. 34, 469–480 (2017).CAS 
    Article 

    Google Scholar 
    47.Lutz, G., Chavarría, M., Arias, M. L. & Mata-Segreda, J. F. Microbial degradation of palm (Elaeis guineensis) biodiesel. Rev. Biol. Trop. 54, 59–63 (2006).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    48.Holmes, A. J. et al. Diverse, yet-to-be-cultured members of the Rubrobacter subdivision of the Actinobacteria are widespread in Australian arid soils. FEMS Microbiol. Ecol. 33, 111–120 (2000).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    49.Wollherr, A. et al. Pyrosequencing-based assessment of bacterial community structure along different management types in German forest and grassland soils. PLoS ONE 6, 1–12 (2011).
    Google Scholar 
    50.Crampon, M., Bodilis, J. & Portet-Koltalo, F. Linking initial soil bacterial diversity and polycyclic aromatic hydrocarbons (PAHs) degradation potential. J. Hazard. Mater. 359, 500–509 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    51.Wang, L., Li, F., Zhan, Y. & Zhu, L. Shifts in microbial community structure during in situ surfactant-enhanced bioremediation of polycyclic aromatic hydrocarbon-contaminated soil. Environ. Sci. Pollut. Res. 23, 14451–14461 (2016).CAS 
    Article 

    Google Scholar 
    52.van Beilen, J. B., Kingma, J. & Witholt, B. Substrate specificity of the alkane hydroxylase system of Pseudomonas oleovorans GPo1. Enzyme Microb. Technol. 16, 904–911 (1994).Article 

    Google Scholar 
    53.Mukherjee, A. et al. Bioinformatic approaches including predictive metagenomic profiling reveal characteristics of bacterial response to petroleum hydrocarbon contamination in diverse environments. Sci. Rep. 7, 1108 (2017).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    54.Ono, K., Nozaki, M. & Hayaishi, O. Purification and some properties of protocatechuate 4,5-dioxygenase. Biochim. Biophys. Acta Enzymol. 220, 224–238 (1970).CAS 
    Article 

    Google Scholar 
    55.Fung, H. K. H. et al. Biochemical and biophysical characterisation of haloalkane dehalogenases DmrA and DmrB in Mycobacterium strain JS60 and their role in growth on haloalkanes. Mol. Microbiol. 97, 439–453 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    56.Kang, Y.-S. & Park, W. Protection against diesel oil toxicity by sodium chloride-induced exopolysaccharides in Acinetobacter sp. strain DR1. J. Biosci. Bioeng. 109, 118–123 (2010).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    57.Ramadass, K., Megharaj, M., Venkateswarlu, K. & Naidu, R. Ecotoxicity of measured concentrations of soil-applied diesel: Effects on earthworm survival, dehydrogenase, urease and nitrification activities. Appl. Soil Ecol. 119, 1–7 (2017).Article 

    Google Scholar 
    58.Moreno, R. & Rojo, F. Enzymes for aerobic degradation of alkanes in bacteria. In Aerobic Utilization of Hydrocarbons, Oils and Lipids (ed. Rojo, F.) 1–25 (Springer, 2017).
    Google Scholar 
    59.Mitter, E. K., de Freitas, J. R. & Germida, J. J. Hydrocarbon-degrading genes in root endophytic communities on oil sands reclamation covers. Int. J. Phytoremediat. 22, 703–712 (2020).CAS 
    Article 

    Google Scholar 
    60.Mitter, E. K., Kataoka, R., de Freitas, J. R. & Germida, J. J. Potential use of endophytic root bacteria and host plants to degrade hydrocarbons. Int. J. Phytoremediat. 21, 928–938 (2019).CAS 
    Article 

    Google Scholar 
    61.Rojo, F. Degradation of alkanes by bacteria: Minireview. Environ. Microbiol. 11, 2477–2490 (2009).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    62.Dincer, K. Lower emissions from biodiesel combustion. Energy Sources A Recov. Util. Environ. Eff. 30, 963–968 (2008).CAS 
    Article 

    Google Scholar 
    63.Miri, M., Bambai, B., Tabandeh, F., Sadeghizadeh, M. & Kamali, N. Production of a recombinant alkane hydroxylase (AlkB2) from Alcanivorax borkumensis. Biotechnol. Lett. 32, 497–502 (2010).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    64.Schomburg, D. & Stephan, D. Rubredoxin-NAD+ reductase. In Enzyme Handbook (eds Schomburg, D. & Stephan, D.) 917–920 (Springer, 1994).
    Google Scholar 
    65.Eggink, G., Engel, H., Vriend, G., Terpstra, P. & Witholt, B. Rubredoxin reductase of Pseudomonas oleovorans. J. Mol. Biol. 212, 135–142 (1990).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    66.Hagelueken, G. et al. Crystal structure of the electron transfer complex rubredoxin rubredoxin reductase of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. 104, 12276–12281 (2007).ADS 
    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    67.Lyu, Y., Zheng, W., Zheng, T. & Tian, Y. Biodegradation of polycyclic aromatic hydrocarbons by Novosphingobium pentaromativorans US6-1. PLoS ONE 9, e101438 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    68.Wang, J. et al. Comparative genomics of degradative Novosphingobium strains with special reference to microcystin-degrading Novosphingobium sp. THN1. Front. Microbiol. 9, 1–17 (2018).Article 

    Google Scholar 
    69.Dhillon, G. S., Amichev, B. Y., de Freitas, J. R. & van Rees, K. Accurate and precise measurement of organic carbon content in carbonate-rich soils. Commun. Soil Sci. Plant Anal. 3624, 2707–2720 (2015).Article 
    CAS 

    Google Scholar 
    70.McKeague, J. A. Manual on SOIL sampling and Methods of Analysis (Canadian Society of Soil Science, 1978).
    Google Scholar 
    71.Laverty, D. H. & Bollo-Kamara, A. Recommended Methods of Soil Analysis for Canadian Prairie Agricultural Soils (Alberta Agriculture, 1988).
    Google Scholar 
    72.Qian, P., Schoenaru, J. J. & Karamanos, R. E. Simultaneous extraction of available phosphorus and potassium with a new soil test: A modification of Kelowna extraction. Commun. Soil Sci. Plant Anal. 25, 627–635 (1994).CAS 
    Article 

    Google Scholar 
    73.Anderson, J. P. E. & Domsch, K. H. A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biol. Biochem. 10, 215–221 (1978).CAS 
    Article 

    Google Scholar 
    74.de Freitas, J. R., Schoenau, J. J., Boyetchko, S. M. & Cyrenne, S. A. Soil microbial populations, community composition, and activity as affected by repeated applications of hog and cattle manure in eastern Saskatchewan. Can. J. Microbiol. 49, 538–548 (2003).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    75.Ramirez, K. S., Craine, J. M. & Fierer, N. Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes. Glob. Change Biol. 18, 1918–1927 (2012).ADS 
    Article 

    Google Scholar 
    76.Craine, J. M., Fierer, N. & McLauchlan, K. K. Widespread coupling between the rate and temperature sensitivity of organic matter decay. Nat. Geosci. 3, 854–857 (2010).ADS 
    CAS 
    Article 

    Google Scholar 
    77.Helgason, B. L., Walley, F. L. & Germida, J. J. Long-term no-till management affects microbial biomass but not community composition in Canadian prairie agroecosytems. Soil Biol. Biochem. 42, 2192–2202 (2010).CAS 
    Article 

    Google Scholar 
    78.Drenovsky, R. E., Elliott, G. N., Graham, K. J. & Scow, K. M. Comparison of phospholipid fatty acid (PLFA) and total soil fatty acid methyl esters (TSFAME) for characterizing soil microbial communities. Soil Biol. Biochem. 36, 1793–1800 (2004).CAS 
    Article 

    Google Scholar 
    79.Macdonald, L. M., Paterson, E., Dawson, L. A. & McDonald, A. J. S. Short-term effects of defoliation on the soil microbial community associated with two contrasting Lolium perenne cultivars. Soil Biol. Biochem. 36, 489–498 (2004).CAS 
    Article 

    Google Scholar 
    80.Zelles, L., Bai, Q. Y., Beck, T. & Beese, F. Signature fatty acids in phospholipids and lipopolysaccharides as indicators of microbial biomass and community structure in agricultural soils. Soil Biol. Biochem. 24, 317–323 (1992).CAS 
    Article 

    Google Scholar 
    81.Hynes, H. M. & Germida, J. J. Relationship between ammonia oxidizing bacteria and bioavailable nitrogen in harvested forest soils of central Alberta. Soil Biol. Biochem. 46, 18–25 (2012).CAS 
    Article 

    Google Scholar 
    82.McCune, B. & Mefford, M. J. Multivariate analysis of Ecological Data (2011).83.Helgason, B. L., Walley, F. L. & Germida, J. J. No-till soil management increases microbial biomass and alters community profiles in soil aggregates. Appl. Soil Ecol. 46, 390–397 (2010).Article 

    Google Scholar 
    84.McCune, B. & Grace, J. B. Analysis of Ecological Communities (2002).85.Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    86.Boylen, E. et al. QIIME 2: Reproducible, interactive, scalable, and extensible microbiome data science. PeerJ Prepr. https://doi.org/10.7287/peerj.preprints.27295 (2018).Article 

    Google Scholar 
    87.Caporaso, J. G. et al. Moving pictures of the human microbiome. Genome Biol. 12, 1–8 (2011).Article 

    Google Scholar 
    88.Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    89.Anderson, M. J. A new method for non-parametric multivariate analysis of variance. Austral. Ecol. 26, 32–46 (2001).
    Google Scholar 
    90.Oksanen, J. et al. Community Ecology Package ‘vegan’ (2020).91.Hamilton, N. ggtern: An Extension to ‘ggplot2’, for the Creation of Ternary Diagrams (2018).92.Douglas, G. M. et al. PICRUSt2 for prediction of metagenome functions. Nat. Biotechnol. 38, 685–688 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    93.Langille, M. G. I. et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 31, 814–821 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    94.Kanehisa, M., Sato, Y., Furumichi, M., Morishima, K. & Tanabe, M. New approach for understanding genome variations in KEGG. Nucleic Acids Res. 47, D590–D595 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    95.Parks, D. H. & Beiko, R. G. Identifying biologically relevant differences between metagenomic communities. Bioinformatics 26, 715–721 (2010).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar  More

  • in

    Heterogeneity in patterns of helminth infections across populations of mountain gorillas (Gorilla beringei beringei)

    1.Weber, A. W. & Vedder, A. Population dynamics of the Virunga gorillas: 1959–1978. Biol. Conserv. 26, 341–366 (1983).Article 

    Google Scholar 
    2.Granjon, A.-C. et al. Estimating abundance and growth rates in a wild mountain gorilla population. Anim. Conserv. 23, 455–465 (2020).Article 

    Google Scholar 
    3.Gray, M. et al. Virunga Massif Mountain Gorilla Census—2010 Summary Report (IGCP & Partners, 2010).
    Google Scholar 
    4.Gray, M. et al. Genetic census reveals increased but uneven growth of a critically endangered mountain gorilla population. Biol. Conserv. 158, 230–238 (2013).Article 

    Google Scholar 
    5.Robbins, M. M. et al. Extreme conservation leads to recovery of the Virunga mountain gorillas. PLoS One 6, e19788 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    6.Hickey, J. R., Granjon, A.-C. & Vigilant, L. Virunga 2015–2016 Surveys: Monitoring Mountain Gorillas, Other Select Mammals, and Illegal Activities (IGCP & Partners, 2019).
    Google Scholar 
    7.Kalpers, J. et al. Gorillas in the crossfire: Population dynamics of the Virunga mountain gorillas over the past three decades. Oryx 37, 326–337 (2003).Article 

    Google Scholar 
    8.Robbins, M. M., Gray, M., Kagoda, E. & Robbins, A. M. Population dynamics of the Bwindi mountain gorillas. Biol. Conserv. 142, 2886–2895 (2009).Article 

    Google Scholar 
    9.Hickey, J. R., Uzabaho, E. & Akantorana, M. Bwindi-Sarambwe EM 2018 Surveys: Monitoring Mountain Gorillas, Other Select Mammals, and Human Activities 40 (GVTC, IGCP & Partners, 2019).
    Google Scholar 
    10.Roy, J. et al. Challenges in the use of genetic mark-recapture to estimate the population size of Bwindi mountain gorillas (Gorilla beringei beringei). Biol. Conserv. 180, 249–261 (2014).Article 

    Google Scholar 
    11.McNeilage, A. J. Mountain Gorillas in the Virunga Volcanoes: Ecology and Carrying Capacity (University of Bristol, 1995).
    Google Scholar 
    12.Caillaud, D., Ndagijimana, F., Giarrusso, A. J., Vecellio, V. & Stoinski, T. S. Mountain gorilla ranging patterns: Influence of group size and group dynamics. Am. J. Primatol. 76, 730–746 (2014).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    13.Caillaud, D. et al. Violent encounters between social units hinder the growth of a high-density mountain gorilla population. Sci. Adv. 6, eaba0724 (2020).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    14.Watts, D. P. Causes and consequences of variation in male mountain gorilla life histories and group membership. In Primate Males (ed. Kappeler, P. M.) 169–179 (Cambridge University Press, 2000).
    Google Scholar 
    15.Robbins, M. M., Robbins, A. M., Gerald-Steklis, N. & Steklis, H. D. Socioecological influences on the reproductive success of female mountain gorillas (Gorilla beringei beringei). Behav. Ecol. Sociobiol. 61, 919–931 (2007).Article 

    Google Scholar 
    16.Robbins, A. M. et al. Impact of male Infanticide on the social structure of mountain gorillas. PLoS One 8, e78256 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    17.Grueter, C. C. et al. Quadratic relationships between group size and foraging efficiency in a herbivorous primate. Sci. Rep. 8, 16718 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    18.Eckardt, W., Stoinski, T. S., Rosenbaum, S. & Santymire, R. Social and ecological factors alter stress physiology of Virunga mountain gorillas (Gorilla beringei beringei). Ecol. Evol. 9, 5248–5259 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    19.Harcourt, A. H., Parks, S. A. & Woodroffe, R. Human density as an influence on species/area relationships: Double jeopardy for small African reserves?. Biodivers. Conserv. 10, 1011–1026 (2001).Article 

    Google Scholar 
    20.Citterio, C. V. et al. Abomasal nematode community in an alpine chamois (Rupicapra r. rupicapra) population before and after a die-off. J. Parasitol. 92, 918–927 (2006).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    21.Hudson, P. J. Macroparasites: Observed patterns. Ecol. Infect. Dis. Nat. Popul. 20, 144–176 (1995).
    Google Scholar 
    22.Albon, S. D. et al. The role of parasites in the dynamics of a reindeer population. Proc. R. Soc. Lond. B Biol. Sci. 269, 1625–1632 (2002).CAS 
    Article 

    Google Scholar 
    23.Anderson, R. M. & May, R. M. Age-related changes in the rate of disease transmission: Implications for the design of vaccination programmes. Epidemiol. Infect. 94, 365–436 (1985).CAS 

    Google Scholar 
    24.Lloyd-Smith, J. O., Schreiber, S. J., Kopp, P. E. & Getz, W. M. Superspreading and the effect of individual variation on disease emergence. Nature 438, 355–359 (2005).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    25.Anderson, R. M. & May, R. M. Regulation and stability of host-parasite population interactions: I. Regulatory processes. J. Anim. Ecol. 47, 219–247 (1978).Article 

    Google Scholar 
    26.Arneberg, P., Skorping, A., Grenfell, B. & Read, A. F. Host densities as determinants of abundance in parasite communities. Proc. R. Soc. Lond. B Biol. Sci. 265, 1283–1289 (1998).Article 

    Google Scholar 
    27.Gillespie, T. R. & Chapman, C. A. Forest fragmentation, the decline of an endangered primate, and changes in host–parasite interactions relative to an unfragmented forest. Am. J. Primatol. 70, 222–230 (2008).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    28.Mbora, D. N. M. & McPeek, M. A. Host density and human activities mediate increased parasite prevalence and richness in primates threatened by habitat loss and fragmentation. J. Anim. Ecol. 78, 210–218 (2009).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    29.dos Santos, C. N. et al. Seasonal dynamics of cyathostomin (Nematoda–Cyathostominae) infective larvae in Brachiaria humidicola grass in tropical southeast Brazil. Vet. Parasitol. 180, 274–278 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    30.Silangwa, S. M. & Todd, A. C. Vertical migration of trichostrongylid larvae on grasses. J. Parasitol. 50, 278–285 (1964).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    31.Callinan, A. P. L. & Westcott, J. M. Vertical distribution of trichostrongylid larvae on herbage and in soil. Int. J. Parasitol. 16, 241–244 (1986).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    32.Crofton, H. D. The ecology of immature phases of trichostrongyle nematodes: II. The effect of climatic factors on the availability of the infective larvae of Trichostrongylus retortaeformis to the host. Parasitology 39, 26–38 (1948).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    33.Zanet, S. et al. Higher risk of gastrointestinal parasite infection at lower elevation suggests possible constraints in the distributional niche of Alpine marmots. PLoS One 12, e0182477 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    34.Derek Scasta, J. Livestock parasite management on high-elevation rangelands: Ecological interactions of climate, habitat, and wildlife. J. Integr. Pest Manag. 6, 20 (2015).Article 

    Google Scholar 
    35.Huffman, M. A., Gotoh, S., Turner, L. A., Hamai, M. & Yoshida, K. Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains, Tanzania. Primates 38, 111–125 (1997).Article 

    Google Scholar 
    36.MacIntosh, A. J. J., Hernandez, A. D. & Huffman, M. A. Host age, sex, and reproductive seasonality affect nematode parasitism in wild Japanese macaques. Primates 51, 353–364 (2010).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    37.Pafčo, B. et al. Do habituation, host traits and seasonality have an impact on protist and helminth infections of wild western lowland gorillas?. Parasitol. Res. 116, 3401–3410 (2017).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    38.Rothman, J. M., Pell, A. N. & Bowman, D. D. Host-parasiteecology of the helminths in mountain gorillas. J. Parasitol. 94, 834–840 (2008).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    39.Müller-Graf, C. D. M., Collins, D. A. & Woolhouse, M. E. J. Intestinal parasite burden in five troops of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. Parasitology 112, 489–497 (1996).PubMed 
    Article 

    Google Scholar 
    40.Alexander, J. & Stimson, W. H. Sex hormones and the course of parasitic infection. Parasitol. Today 4, 189–193 (1988).Article 

    Google Scholar 
    41.Bundy, D. A. P. Gender-dependent patterns of infections and disease. Parasitol. Today 4, 186–189 (1988).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    42.Zuk, M. Reproductive strategies and disease susceptibility: An evolutionary viewpoint. Parasitol. Today 6, 231–233 (1990).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    43.Nunn, C. & Altizer, S. Infectious Diseases in Primates: Behavior (Ecology and Evolution. Oxford University Press, Oxford, 2006).Book 

    Google Scholar 
    44.Wilson, K. et al. Heterogeneities in macroparasite infections: Patterns and processes. In The Ecology of Wildlife Diseases 6–44 (2002).45.Cattadori, I. M., Boag, B., Bjørnstad, O. N., Cornell, S. J. & Hudson, P. J. Peak shift and epidemiology in a seasonal host–nematode system. Proc. R. Soc. B Biol. Sci. 272, 1163–1169 (2005).CAS 
    Article 

    Google Scholar 
    46.Terio, K. A. et al. Oesophagostomiasis in non-human primates of Gombe National Park, Tanzania. Am. J. Primatol. 80, e22572 (2018).Article 

    Google Scholar 
    47.Gillespie, T. R., Nunn, C. L. & Leendertz, F. H. Integrative approaches to the study of primate infectious disease: Implications for biodiversity conservation and global health. Am. J. Phys. Anthropol. 137, 53–69 (2008).Article 

    Google Scholar 
    48.Collett, M. G. et al. Gastric Ollulanus tricuspis infection identified in captive cheetahs (Acinonyx jubatus) with chronic vomiting: Case report. J. S. Afr. Vet. Assoc. 71, 251–255 (2000).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    49.Dennis, M. M., Bennett, N. & Ehrhart, E. J. Gastric adenocarcinoma and chronic gastritis in two related Persian cats. Vet. Pathol. 43, 358–362 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    50.Smetana, H. F. & Orihel, T. C. Gastric papillomata in Macaca speciosa induced by Nochtia nochti (Nematoda: Trichostrongyloidea). J. Parasitol. 55, 349–351 (1969).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    51.Nybelin, O. Anoplocephala gorillae n. sp. Ark Zool. 19, 1–3 (1924).
    Google Scholar 
    52.Sleeman, J. M., Meader, L. L., Mudakikwa, A. B., Foster, J. W. & Patton, S. Gastrointestinal parasites of mountain gorillas (Gorilla gorilla beringei) in the Parc National des Volcans, Rwanda. J. Zool. Wildl. Med. 31, 322–328 (2000).CAS 
    Article 

    Google Scholar 
    53.Ashford, R. W., Lawson, H., Butynski, T. M. & Reid, G. D. F. Patterns of intestinal parasitism in the mountain gorilla Gorilla gorilla in the Bwindi-Impenetrable Forest, Uganda. J. Zool. 239, 507–514 (1996).Article 

    Google Scholar 
    54.Kalema-Zikusoka, G., Rothman, J. M. & Fox, M. T. Intestinal parasites and bacteria of mountain gorillas (Gorilla beringei beringei) in Bwindi Impenetrable National Park, Uganda. Primates 46, 59–63 (2005).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    55.Owiunji, I, et al. The biodiversity of the Virunga Volcanoes. https://programs.wcs.org/portals/49/media/file/volcanoes_biodiv_survey.pdf (2005).56.Langdale-Brown, I., Osmaston, H. & Wilson, J. G. The Vegetation of Uganda and Its Bearing on Land-Use (Governmentt of Uganda, 1964).
    Google Scholar 
    57.Ashford, R. W., Reid, G. D. F. & Butynski, T. M. The intestinal faunas of man and mountain gorillas in a shared habitat. Ann. Trop. Med. Parasitol. 84, 337–340 (1990).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    58.Shutt, K. et al. Effects of habituation, research and ecotourism on faecal glucocorticoid metabolites in wild western lowland gorillas: Implications for conservation management. Biol. Conserv. 172, 72–79 (2014).Article 

    Google Scholar 
    59.Kayiranga, A. et al. Analysis of climate and topography impacts on the spatial distribution of vegetation in the Virunga Volcanoes Massif of East-Central Africa. Geosciences 7, 17 (2017).ADS 
    Article 

    Google Scholar 
    60.Cousins, D. & Huffman, M. A. Medicinal properties in the diet of gorillas: An ethno-phramacological evaluation. Afr. Stud. Monogr. 23, 65–89 (2002).
    Google Scholar 
    61.Woolhouse, M. E. J. Patterns in parasite epidemiology: The peak shift. Parasitol. Today 14, 428–434 (1998).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    62.Hayes, K. S., Bancroft, A. J. & Grencis, R. K. Immune-mediated regulation of chronic intestinal nematode infection. Immunol. Rev. 201, 75–88 (2004).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    63.Maizels, R. M. et al. Helminth parasites—masters of regulation. Immunol. Rev. 201, 89–116 (2004).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    64.Proudman, C. J., Holmes, M. A., Sheoran, A. S., Edwards, S. E. R. & Trees, A. J. Immunoepidemiology of the equine tapeworm Anoplocephala perfoliata: Age-intensity profile and age-dependency of antibody subtype responses. Parasitology 114, 89–94 (1997).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    65.Gergócs, V., Garamvölgyi, Á., Homoródi, R. & Hufnagel, L. Seasonal change of oribatid mite communities (Acari, Oribatida) in three different types of microhabitats in an oak forest. Appl. Ecol. Environ. Res. 9, 181–195 (2011).Article 

    Google Scholar 
    66.Dobson, A. & Foufopoulos, J. Emerging infectious pathogens of wildlife. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 356, 1001–1012 (2001).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    67.Xue, Y. et al. Mountain gorilla genomes reveal the impact of long-term population decline and inbreeding. Science 348, 242–245 (2015).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    68.Reed, D. H. & Frankham, R. Correlation between fitness and genetic diversity. Conserv. Biol. 17, 230–237 (2003).Article 

    Google Scholar 
    69.Pafčo, B. et al. Metabarcoding analysis of strongylid nematode diversity in two sympatric primate species. Sci. Rep. 8, 5933 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    70.McNeilage, A. Diet and habitat use of two mountain gorilla groups in contrasting habitats in the Virunga. In Mountain Gorillas: Three Decades of Research at Karisoke (Cambridge University Press, 2001).
    Google Scholar 
    71.Sinayitutse, E. et al. Daily defecation outputs of mountain gorillas (Gorilla beringei beringei) in the Volcanoes National Park, Rwanda. Primates https://doi.org/10.1007/s10329-020-00874-7 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    72.Burgunder, J. et al. Complexity in behavioural organization and strongylid infection among wild chimpanzees. Anim. Behav. 129, 257–268 (2017).Article 

    Google Scholar 
    73.Chapman, C. A., Speirs, M. L., Gillespie, T. R., Holland, T. & Austad, K. M. Life on the edge: Gastrointestinal parasites from the forest edge and interior primate groups. Am. J. Primatol. 68, 397–409 (2006).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    74.Anderson, R. M. & Schad, G. A. Hookworm burdens and faecal egg counts: An analysis of the biological basis of variation. Trans. R. Soc. Trop. Med. Hyg. 79, 812–825 (1985).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    75.Warnick, L. D. Daily variability of equine fecal strongyle egg counts. Cornell Vet. 82, 453–463 (1992).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    76.Tomczuk, K. et al. Comparison of the sensitivity of coprological methods in detecting Anoplocephala perfoliata invasions. Parasitol. Res. 113, 2401–2406 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    77.Williamson, R., Beveridge, I. & Gasser, R. Coprological methods for the diagnosis of Anoplocephala perfoliata infection of the horse. Aust. Vet. J. 76, 618–621 (1998).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    78.Cringoli, G. et al. The Mini-FLOTAC technique for the diagnosis of helminth and protozoan infections in humans and animals. Nat. Protoc. 12, 1723–1732 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    79.Guschanski, K. et al. Counting elusive animals: Comparing field and genetic census of the entire mountain gorilla population of Bwindi Impenetrable National Park, Uganda. Biol. Conserv. 142, 290–300 (2009).Article 

    Google Scholar 
    80.Zuur, A., Ieno, E. N., Walker, N., Saveliev, A. A. & Smith, G. M. Mixed Effects Models and Extensions in Ecology with R (Springer, 2009).MATH 
    Book 

    Google Scholar 
    81.Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).Article 

    Google Scholar 
    82.R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (2020).83.Forstmeier, W. & Schielzeth, H. Cryptic multiple hypotheses testing in linear models: Overestimated effect sizes and the winner’s curse. Behav. Ecol. Sociobiol. 65, 47–55 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    84.Engqvist, L. The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim. Behav. 70, 20 (2005).Article 

    Google Scholar 
    85.Gelman, A. & Hill, J. Data Analysis Using Regression and Multilevel/Hierarchical Models (Cambridge University Press, 2007).
    Google Scholar 
    86.Schielzeth, H. Simple means to improve the interpretability of regression coefficients. Methods Ecol. Evol. 1, 103–113 (2010).Article 

    Google Scholar 
    87.Johnson, J. B. & Omland, K. S. Model selection in ecology and evolution. Trends Ecol. Evol. 19, 101–108 (2004).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    88.Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach (Springer, 2002).MATH 

    Google Scholar 
    89.Barton, K. MuMIn: Multi-Model Inference. R package version 1.43.17. https://CRAN.R-project.org/package=MuMIn (2020). More

  • in

    Correction: Gulf of Mexico blue hole harbors high levels of novel microbial lineages

    N. V. PatinPresent address: Ocean Chemistry and Ecosystems Division, Atlantic Oceanographic and Meteorological Laboratory, National Oceanic and Atmospheric Administration, Miami, FL, USAN. V. PatinPresent address: Cooperative Institute for Marine and Atmospheric Studies, Rosenstiel School of Marine and Atmospheric Science, University of Miami, Miami, FL, USAN. V. PatinPresent address: Stationed at Southwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, La Jolla, CA, USASchool of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, USAN. V. Patin & F. J. StewartCenter for Microbial Dynamics and Infection, Georgia Institute of Technology, Atlanta, GA, USAN. V. Patin & F. J. StewartBowdoin College, Brunswick, ME, USAZ. A. DietrichHarbor Branch Oceanographic Institute, Florida Atlantic University, Ft. Pierce, FL, USAA. Stancil, M. Quinan & J. S. BecklerMote Marine Laboratory, Sarasota, FL, USAE. R. Hall & J. CulterU.S. Geological Survey, St. Petersburg Coastal and Marine Science Center, St. Petersburg, FL, USAC. G. SmithSchool of Earth & Atmospheric Sciences, Georgia Institute of Technology, Atlanta, GA, USAM. TaillefertDepartment of Microbiology & Immunology, Montana State University, Bozeman, MT, USAF. J. Stewart More

  • in

    The chosen few—variations in common and rare soil bacteria across biomes

    1.Nemergut DR, Schmidt SK, Fukami T, O’Neill SP, Bilinski TM, Stanish LF, et al. Patterns and processes of microbial community assembly. Microbiol Mol Biol Rev. 2013;77:342–56.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    2.Jousset A, Bienhold C, Chatzinotas A, Gallien L, Gobet A, Kurm V, et al. Where less may be more: how the rare biosphere pulls ecosystems strings. ISME J. 2017;11:853–62.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    3.Rivett DW, Bell T. Abundance determines the functional role of bacterial phylotypes in complex communities. Nat Microbiol. 2018;3:767–72.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    4.Bell T, Newman JA, Silverman BW, Turner SL, Lilley AK. The contribution of species richness and composition to bacterial services. Nature. 2005;436:1157–60.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    5.Starke R, Capek P, Morais D, Callister SJ, Jehmlich N. The total microbiome functions in bacteria and fungi. J Proteom. 2020;213:1–5.Article 
    CAS 

    Google Scholar 
    6.Saleem M, Hu J, Jousset A. More than the sum of its parts: microbiome biodiversity as a driver of plant growth and soil health. Annu Rev Ecol Evol Syst. 2019;50:145–68.Article 

    Google Scholar 
    7.Wagg C, Schlaeppi K, Banerjee S, Kuramae EE, Heijden van der MGA. Fungal-bacterial diversity and microbiome complexity predict ecosystem functioning. Nat Commun. 2019;10:1–10.CAS 
    Article 

    Google Scholar 
    8.Delgado-Baquerizo M, Maestre FT, Reich PB, Jeffries TC, Gaitan JJ, Encinar D, et al. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat Commun. 2016;7:1–8.Article 
    CAS 

    Google Scholar 
    9.Delgado-Baquerizo M, Reich PB, Trivedi C, Eldridge DJ, Abades S, Alfaro FD, et al. Multiple elements of soil biodiversity drive ecosystem functions across biomes. Nat Ecol Evol. 2020;4:210–20.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    10.Aanderud ZT, Jones SE, Fierer N, Lennon JT. Resuscitation of the rare biosphere contributes to pulses of ecosystem activity. Front Microbiol. 2015;6:1–11.Article 

    Google Scholar 
    11.Song H-K, Song W, Kim M, Tripathi BM, Kim H, Jablonski P, et al. Bacterial strategies along nutrient and time gradients, revealed by metagenomic analysis of laboratory microcosms. FEMS Microbiol Ecol. 2017;93:1–13.Article 
    CAS 

    Google Scholar 
    12.Jiao S, Chen W, Wei G. Biogeography and ecological diversity patterns of rare and abundant bacteria in oil-contaminated soils. Mol Ecol. 2017;26:5305–5317.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    13.Delgado-Baquerizo M, Oliverio AM, Brewer TE, Benavent-González A, Eldridge DJ, Bardgett RD, et al. A global atlas of the dominant bacteria found in soil. Science. 2018;359:320–5.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    14.Yu X, Polz MF, Alm EJ. Interactions in self-assembled microbial communities saturate with diversity. ISME J. 2019;13:1602–17.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    15.Li P, Liu J, Jiang C, Wu M, Liu M, Li Z. Distinct successions of common and rare bacteria in soil under humic acid amendment—a microcosm study. Front Microbiol. 2019;10:1–14.Article 

    Google Scholar 
    16.Nemergut DR, Costello EK, Hamady M, Lozupone C, Jiang L, Schmidt SK, et al. Global patterns in the biogeography of bacterial taxa. Environ Microbiol. 2011;13:135–44.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    17.Bickel S, Chen X, Papritz A, Or D. A hierarchy of environmental covariates control the global biogeography of soil bacterial richness. Sci Rep. 2019;9:1–10.CAS 
    Article 

    Google Scholar 
    18.Clarke RT, Murphy JF. Effects of locally rare taxa on the precision and sensitivity of RIVPACS bioassessment of freshwaters. Freshw Biol. 2006;51:1924–40.Article 

    Google Scholar 
    19.Kurm V, Putten WH, van der, Boer W, de, Naus‐Wiezer S, Hol WHG. Low abundant soil bacteria can be metabolically versatile and fast growing. Ecology. 2017;98:555–64.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    20.Kurm V, Putten WH, van der, Hol WHG. Cultivation-success of rare soil bacteria is not influenced by incubation time and growth medium. PLoS ONE. 2019;14:1–14.Article 
    CAS 

    Google Scholar 
    21.Meyer KM, Memiaghe H, Korte L, Kenfack D, Alonso A, Bohannan BJM. Why do microbes exhibit weak biogeographic patterns? ISME J. 2018;12:1404–13.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    22.Escalas A, Hale L, Voordeckers JW, Yang Y, Firestone MK, Alvarez‐Cohen L, et al. Microbial functional diversity: from concepts to applications. Ecol Evol. 2019;9:12000–16.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    23.Barberán A, Ramirez KS, Leff JW, Bradford MA, Wall DH, Fierer N. Why are some microbes more ubiquitous than others? Predicting the habitat breadth of soil bacteria. Ecol Lett. 2014;17:794–802.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    24.Dee LE, Cowles J, Isbell F, Pau S, Gaines SD, Reich PB. When do ecosystem services depend on rare species? Trends Ecol Evol. 2019;34:746–58.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    25.Pueyo S, He F, Zillio T. The maximum entropy formalism and the idiosyncratic theory of biodiversity. Ecol Lett. 2007;10:1017–28.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    26.Bahram M, Hildebrand F, Forslund SK, Anderson JL, Soudzilovskaia NA, Bodegom PM, et al. Structure and function of the global topsoil microbiome. Nature. 2018;560:233–7.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    27.Zhou J, Deng Y, Shen L, Wen C, Yan Q, Ning D, et al. Temperature mediates continental-scale diversity of microbes in forest soils. Nat Commun. 2016;7:1–10.
    Google Scholar 
    28.Thompson LR, Jex AR, Campbell AH, Linz AM, Berry A, Williams AE, et al. A communal catalogue reveals Earth’s multiscale microbial diversity. Nature. 2017;551:457–63.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    29.Bickel S, Or D. Soil bacterial diversity mediated by microscale aqueous-phase processes across biomes. Nat Commun. 2020;11:1–9.
    Google Scholar 
    30.Xu X, Thornton PE, Post WM. A global analysis of soil microbial biomass carbon, nitrogen and phosphorus in terrestrial ecosystems. Glob Ecol Biogeogr. 2013;22:737–49.Article 

    Google Scholar 
    31.Serna-Chavez HM, Fierer N, van Bodegom PM. Global drivers and patterns of microbial abundance in soil: global patterns of soil microbial biomass. Glob Ecol Biogeogr. 2013;22:1162–72.Article 

    Google Scholar 
    32.Wang G, Or D. A hydration-based biophysical index for the onset of soil microbial coexistence. Sci Rep. 2012;2:1–5.
    Google Scholar 
    33.Li CH, Lee CK. Minimum cross entropy thresholding. Pattern Recognit. 1993;26:617–625.Article 

    Google Scholar 
    34.Walt S, van der, Schönberger JL, Nunez-Iglesias J, Boulogne F, Warner JD, Yager N, et al. scikit-image: image processing in Python. PeerJ. 2014;2:1–18.
    Google Scholar 
    35.Homem-de-Mello T, Rubinstein RY. Estimation of rare event probabilities using cross-entropy. Proc Winter Simul Conf. 2002;1:310–19.Article 

    Google Scholar 
    36.Murali A, Bhargava A, Wright ES. IDTAXA: a novel approach for accurate taxonomic classification of microbiome sequences. Microbiome. 2018;6:1–14.Article 

    Google Scholar 
    37.Šťovíček A, Kim M, Or D, Gillor O. Microbial community response to hydration-desiccation cycles in desert soil. Sci Rep. 2017;7:1–9.Article 
    CAS 

    Google Scholar 
    38.Zhao M, Heinsch FA, Nemani RR, Running SW. Improvements of the MODIS terrestrial gross and net primary production global data set. Remote Sens Environ. 2005;95:164–76.Article 

    Google Scholar 
    39.Fick SE, Hijmans RJ. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas: new climate surfaces for global land areas. Int J Climatol. 2017;37:4302–15.Article 

    Google Scholar 
    40.Schoolfield RM, Sharpe PJH, Magnuson CE. Non-linear regression of biological temperature-dependent rate models based on absolute reaction-rate theory. J Theor Biol. 1981;88:719–31.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    41.Beck HE, Wood EF, Pan M, Fisher CK, Miralles DG, van Dijk AIJM, et al. MSWEP V2 Global 3-hourly 0.1° precipitation: methodology and quantitative assessment. Bull Am Meteorol Soc. 2019;100:473–500.Article 

    Google Scholar 
    42.Wang G, Or D. Hydration dynamics promote bacterial coexistence on rough surfaces. ISME J. 2013;7:395–404.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    43.Kim M, Or D. Individual-based model of microbial life on hydrated rough soil surfaces. PLoS ONE. 2016;11:1–31.
    Google Scholar 
    44.Hermsen R, Okano H, You C, Werner N, Hwa T. A growth-rate composition formula for the growth of E.coli on co-utilized carbon substrates. Mol Syst Biol. 2015;11:1–6.Article 
    CAS 

    Google Scholar 
    45.García FC, Bestion E, Warfield R, Yvon-Durocher G. Changes in temperature alter the relationship between biodiversity and ecosystem functioning. Proc Natl Acad Sci. 2018;115:10989–94.PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    46.Slessarev EW, Lin Y, Bingham NL, Johnson JE, Dai Y, Schimel JP, et al. Water balance creates a threshold in soil pH at the global scale. Nature. 2016;540:567–9.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    47.Treves DS, Xia B, Zhou J, Tiedje JM. A two-species test of the hypothesis that spatial isolation influences microbial diversity in soil. Micro Ecol. 2003;45:20–8.CAS 
    Article 

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

    Google Scholar 
    49.Stauffer D. Scaling theory of percolation clusters. Phys Rep. 1979;54:1–74.Article 

    Google Scholar 
    50.Scher H, Zallen R. Critical density in percolation processes. J Chem Phys. 1970;53:3759–61.CAS 
    Article 

    Google Scholar 
    51.Hengl T, de Jesus JM, Heuvelink GB, Gonzalez MR, Kilibarda M, Blagotić A, et al. SoilGrids250m: global gridded soil information based on machine learning. PloS ONE. 2017;12:1–40.Article 
    CAS 

    Google Scholar 
    52.Chase AB, Arevalo P, Brodie EL, Polz MF, Karaoz U, Martiny JBH. Maintenance of sympatric and allopatric populations in free-living terrestrial bacteria. mBio. 2019;10:1–11.Article 

    Google Scholar 
    53.Fisher CK, Mehta P. The transition between the niche and neutral regimes in ecology. Proc Natl Acad Sci. 2014;111:13111–6.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    54.Ratzke C, Barrere J, Gore J. Strength of species interactions determines biodiversity and stability in microbial communities. Nat Ecol Evol. 2020;4:376–83.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    55.Doud DFR, Bowers RM, Schulz F, Raad MD, Deng K, Tarver A, et al. Function-driven single-cell genomics uncovers cellulose-degrading bacteria from the rare biosphere. ISME J. 2020;14:659–75.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    56.Shade A, Jones SE, Caporaso JG, Handelsman J, Knight R, Fierer N, et al. Conditionally rare taxa disproportionately contribute to temporal changes in microbial diversity. mBio. 2014;5:1–9.Article 
    CAS 

    Google Scholar 
    57.Kaminsky R, Morales SE. Conditionally rare taxa contribute but do not account for changes in soil prokaryotic community structure. Front Microbiol. 2018;9:1–6.Article 

    Google Scholar 
    58.Price PB, Sowers T. Temperature dependence of metabolic rates for microbial growth, maintenance, and survival. Proc Natl Acad Sci U S A. 2004;101:4631–6.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

  • in

    Chill coma onset and recovery fail to reveal true variation in thermal performance among populations of Drosophila melanogaster

    1.Addo-Bediako, A., Chown, S. L. & Gaston, K. J. Thermal tolerance, climatic variability and latitude. Proc. R. Soc. B. 267, 739–745 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    2.Andersen, J. L. et al. How to assess Drosophila cold tolerance: chill coma temperature and lower lethal temperature are the best predictors of cold distribution limits. Funct. Ecol. 29, 55–65 (2015).Article 

    Google Scholar 
    3.Kimura, M. T. Cold and heat tolerance of drosophilid flies with reference to their latitudinal distributions. Oecologia 140, 442–449 (2004).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    4.Gaston, K. J. & Chown, S. L. Elevation and climatic tolerance: A test using dung beetles. Oikos 86, 584–590 (1999).Article 

    Google Scholar 
    5.MacMillan, H. A. Dissecting cause from consequence: a systematic approach to thermal limits. J. Exp. Biol. 222, jeb191593 (2019).6.Overgaard, J. & MacMillan, H. A. The integrative physiology of insect chill tolerance. Annu. Rev. Physiol. 79, 187–208 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    7.Armstrong, G. A. B., Rodríguez, E. C. & Meldrum Robertson, R. Cold hardening modulates K+ homeostasis in the brain of Drosophila melanogaster during chill coma. J. Insect Physiol. 58, 1511–1516 (2012).8.Rodgers, C. I., Armstrong, G. A. B. & Robertson, R. M. Coma in response to environmental stress in the locust: a model for cortical spreading depression. J. Insect Physiol. 56, 980–990 (2010).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    9.Andersen, M. K. & Overgaard, J. The central nervous system and muscular system play different roles for chill coma onset and recovery in insects. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 233, 10–16 (2019).10.Koštál, V., Vambera, J. & Bastl, J. On the nature of pre-freeze mortality in insects: Water balance, ion homeostasis and energy charge in the adults of Pyrrhocoris apterus. J. Exp. Biol. 207, 1509–1521 (2004).PubMed 
    Article 

    Google Scholar 
    11.Zachariassen, K. E., Kristiansen, E. & Pedersen, S. A. Inorganic ions in cold-hardiness. Cryobiology 48, 126–133 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    12.MacMillan, H. A. & Sinclair, B. J. The role of the gut in insect chilling injury: Cold-induced disruption of osmoregulation in the fall field cricket, Gryllus pennsylvanicus. J. Exp. Biol. 214, 726–734 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    13.MacMillan, H. A., Williams, C. M., Staples, J. F. & Sinclair, B. J. Reestablishment of ion homeostasis during chill-coma recovery in the cricket Gryllus pennsylvanicus. PNAS 109, 20750–20755 (2012).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    14.MacMillan, H. A., Findsen, A., Pedersen, T. H. & Overgaard, J. Cold-induced depolarization of insect muscle: Differing roles of extracellular K+ during acute and chronic chilling. J. Exp. Biol. 217, 2930–2938 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    15.Bayley, J. S., Sørensen, J. G., Moos, M., Koštál, V. & Overgaard, J. Cold-acclimation increases depolarization resistance and tolerance in muscle fibers from a chill-susceptible insect, Locusta migratoria. Am. J. Physiol. Regul. Integr. Comp. Physiol. 319, R439–R447 (2020).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    16.Bayley, J. S. et al. Cold exposure causes cell death by depolarization-mediated Ca2+ overload in a chill-susceptible insect. PNAS 115, E9737–E9744 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    17.Carrington, J., Andersen, M. K., Brzezinski, K. & MacMillan, H. A. Hyperkalemia, not apoptosis, accurately predicts chilling injury in individual locusts. Proc. R. Soc. B. (in press).18.Koštál, V., Yanagimoto, M. & Bastl, J. Chilling-injury and disturbance of ion homeostasis in the coxal muscle of the tropical cockroach (Nauphoeta cinerea). Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 143, 171–179 (2006).19.MacMillan, H. A., Baatrup, E. & Overgaard, J. Concurrent effects of cold and hyperkalaemia cause insect chilling injury. Proc. R. Soc. B. 282 (2015).20.Garcia, M. J., Littler, A. S., Sriram, A. & Teets, N. M. Distinct cold tolerance traits independently vary across genotypes in Drosophila melanogaster. Evolution 74, 1437–1450 (2020).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    21.Gerken, A. R., Mackay, T. F. C. & Morgan, T. J. Artificial selection on chill-coma recovery time in Drosophila melanogaster: Direct and correlated responses to selection. J. Therm. Biol. 59, 77–85 (2016).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    22.Colinet, H. & Hoffmann, A. A. Comparing phenotypic effects and molecular correlates of developmental, gradual and rapid cold acclimation responses in Drosophila melanogaster. Funct. Ecol. 26, 84–93 (2012).Article 

    Google Scholar 
    23.MacMillan, H. A., Andersen, J. L., Loeschcke, V. & Overgaard, J. Sodium distribution predicts the chill tolerance of Drosophila melanogaster raised in different thermal conditions. Am. J. Physiol. Regul. Integr. Comp. Physiol. 308, R823–R831 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    24.Ransberry, V. E., MacMillan, H. A. & Sinclair, B. J. The relationship between chill-coma onset and recovery at the extremes of the thermal window of Drosophila melanogaster. Physiol. Biochem. Zool. 84, 553–559 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    25.Sunday, J. M., Bates, A. E. & Dulvy, N. K. Global analysis of thermal tolerance and latitude in ectotherms. Proc. R. Soc. B. 278, 1823–1830 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    26.Hoffmann, A. A., Anderson, A. & Hallas, R. Opposing clines for high and low temperature resistance in Drosophila melanogaster. Ecol. Lett. 5, 614–618 (2002).Article 

    Google Scholar 
    27.Hoffmann, A. A., Shirriffs, J. & Scott, M. Relative importance of plastic vs genetic factors in adaptive differentiation: Geographical variation for stress resistance in Drosophila melanogaster from eastern Australia. Funct. Ecol. 19, 222–227 (2005).Article 

    Google Scholar 
    28.Overgaard, J., Hoffmann, A. A. & Kristensen, T. N. Assessing population and environmental effects on thermal resistance in Drosophila melanogaster using ecologically relevant assays. J. Therm. Biol. 36, 409–416 (2011).Article 

    Google Scholar 
    29.Ayrinhac, A. et al. Cold adaptation in geographical populations of Drosophila melanogaster: Phenotypic plasticity is more important than genetic variability. Funct. Ecol. 18, 700–706 (2004).Article 

    Google Scholar 
    30.Gibert, P. & Huey, R. B. Chill-coma temperature in Drosophila: Effects of developmental temperature, latitude, and phylogeny. Physiol. Biochem. Zool. 74, 429–434 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    31.Hori, Y. & Kimura, M. T. Relationship between cold stupor and cold tolerance in Drosophila (Diptera: Drosophilidae). Environ. Entomol. 27, 1297–1302 (1998).Article 

    Google Scholar 
    32.Teets, N. M. & Hahn, D. A. Genetic variation in the shape of cold-survival curves in a single fly population suggests potential for selection from climate variability. J. Evol. Biol. 31, 543–555 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    33.Kellermann, V. et al. Phylogenetic constraints in key functional traits behind species’ climate niches: Patterns of desiccation and cold resistance across 95 Drosophila species. Evolution 66, 3377–3389 (2012).PubMed 
    Article 

    Google Scholar 
    34.Pool, J. E., Braun, D. T. & Lack, J. B. Parallel evolution of cold tolerance within Drosophila melanogaster. Mol. Biol. Evol. 34, 349–360 (2017).CAS 
    PubMed 

    Google Scholar 
    35.Mansourian, S. et al. Wild African Drosophila melanogaster are seasonal specialists on marula fruit. Curr. Biol. 28, 3960-3968.e3 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    36.Pool, J. E. et al. Population genomics of Sub-Saharan Drosophila melanogaster: African diversity and non-African admixture. PLoS Genetics 8, e1003080 (2012).37.Baudry, E., Viginier, B. & Veuille, M. Non-African populations of Drosophila melanogaster have a unique origin. Mol. Biol. Evol. 21, 1482–1491 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    38.MacMillan, H. A., Andersen, J. L., Davies, S. A. & Overgaard, J. The capacity to maintain ion and water homeostasis underlies interspecific variation in Drosophila cold tolerance. Sci. Rep. 5, 18607 (2015).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    39.Chen, C.-P. & Walker, V. K. Cold-shock and chilling tolerance in Drosophila. J. Insect Physiol. 40, 661–669 (1994).Article 

    Google Scholar 
    40.Hoffmann, A. A. & Watson, M. Geographical variation in the acclimation responses of Drosophila to temperature extremes. Am. Nat. 142, S93–S113 (1993).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    41.Ørsted, M., Hoffmann, A. A., Rohde, P. D., Sørensen, P. & Kristensen, T. N. Strong impact of thermal environment on the quantitative genetic basis of a key stress tolerance trait. Heredity 122, 315–325 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    42.Gerken, A. R., Eller, O. C., Hahn, D. A. & Morgan, T. J. Constraints, independence, and evolution of thermal plasticity: probing genetic architecture of long- and short-term thermal acclimation. PNAS 112, 4399–4404 (2015).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    43.Nyamukondiwa, C., Terblanche, J. S., Marshall, K. E. & Sinclair, B. J. Basal cold but not heat tolerance constrains plasticity among Drosophila species (Diptera: Drosophilidae). J. Evol. Biol. 24, 1927–1938 (2011).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    44.van Heerwaarden, B. & Kellermann, V. Does plasticity trade off with basal heat tolerance?. Trends Ecol. Evol. 35, 874–885 (2020).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    45.Gilchrist, G. W., Huey, R. B. & Partridge, L. Thermal sensitivity of Drosophila melanogaster: evolutionary responses of adults and eggs to laboratory natural selection at different temperatures. Physiol. Zool. 70, 403–414 (1997).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    46.Maclean, H. J., Kristensen, T. N., Sørensen, J. G. & Overgaard, J. Laboratory maintenance does not alter ecological and physiological patterns among species: A Drosophila case study. J. Evol. Biol. 31, 530–542 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    47.Henry, Y., Renault, D. & Colinet, H. Hormesis-like effect of mild larval crowding on thermotolerance in Drosophila flies. J. Exp. Biol. 221, jeb169342 (2018).48.Nilson, T. L., Sinclair, B. J. & Roberts, S. P. The effects of carbon dioxide anesthesia and anoxia on rapid cold-hardening and chill coma recovery in Drosophila melanogaster. J. Insect Physiol. 52, 1027–1033 (2006).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    49.Hazell, S. P. & Bale, J. S. Low temperature thresholds: are chill coma and CTmin synonymous?. J. Insect Physiol. 57, 1085–1089 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    50.Bertram, G. C. L. The low temperature limit of activity of arctic insects. J. Anim. Ecol. 4, 35–42 (1935).Article 

    Google Scholar 
    51.Sinclair, B. J., Coello Alvarado, L. E. & Ferguson, L. V. An invitation to measure insect cold tolerance: Methods, approaches, and workflow. J. Therm. Biol. 53, 180–197 (2015).52.MacMillan, H. A. et al. Anti-diuretic activity of a CAPA neuropeptide can compromise Drosophila chill tolerance. J. Exp. Biol. 221, jeb185884 (2018).53.R Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2020). More