More stories

  • in

    Juvenile hormone regulates the shift from migrants to residents in adult oriental armyworm, Mythimna separata

    1.
    Chapman, J. W., Reynolds, D. R. & Wilson, K. Long-range seasonal migration in insects: mechanisms, evolutionary drivers and ecological consequences. Ecol. Lett. 18, 287–302 (2015).
    PubMed  Google Scholar 
    2.
    Zera, A. J. & Tiebel, K. C. Brachypterizing effect of group rearing, juvenile hormone-III, and methoprene on wing length development in the wingdimorphic cricket, Gryllus rubens. J. Insect. Physiol. 34, 489–498 (1988).
    CAS  Google Scholar 

    3.
    Mittler, T. E. Juvenile hormone and aphid polymorphism. In: Morphogenetic Hormones of Arthropods (ed Gupta, A. P.). vol. 3. Rutgers Univ, New Brunswick. 453-474 (1991).

    4.
    Nijhout, H. F. Control mechanisms of polyphenic development in insects. Biosci 49, 181–192 (1999).
    Google Scholar 

    5.
    Rankin, M. A. & Rankin, S. Some factors affecting presumed migratory flight activity of the convergent ladybeetle, Hippodamia convergens (Coccinellidae: Coleoptera). Biol. Bull. 158(3), 356–369 (1980).
    Google Scholar 

    6.
    Wang, F. Y., Zhang, X. X. & Zhai, B. P. Flight and re-migration capacity of the rice leaf folder moth, Cnaphalocrocis medinalis (Guenée) (Lepidoptera: Crambidae). Acta Entomol. Sin 53(11), 1265–1272 (2010).
    Google Scholar 

    7.
    Nakasuji, F. & Nakano, A. Flight activity and oviposition characteristics of the seasonal form of a migrant skipper, Parnara guttata guttata (Lepidoptera: Hesperiidae). Res. Pop. Ecol. 32, 227–233 (1990).
    Google Scholar 

    8.
    Shirai, Y. Flight activity, reproduction, and adult nutrition of the beet webworm, Spoladea recurvalis (Lepidoptera: Pyralidae). Appl. Entomol. Zool. 41, 405–414 (2006).
    Google Scholar 

    9.
    Cheng, Y. X., Luo, L. Z., Jiang, X. F. & Sappington, T. W. Synchronized oviposition triggered by migratory flight intensifies larval outbreaks of beet webworm. PLOS ONE 7, e31562, https://doi.org/10.1371/journal.pone.0031562 (2012).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    10.
    Zhang, L., Pan, P., Sappington, T. W., Lu, W. X. & Luo, L. Z. Accelerated and synchronized oviposition induced by flight of young females may intensify larval outbreaks of the rice leaf roller. PLoS ONE. 8(5), e63554 (2015).
    Google Scholar 

    11.
    Zera, A. J. & Denno, R. F. Physiology and ecology of dispersal polymorphism in insects. Annu. Rev. Entomol. 42, 207–231 (1997).
    CAS  PubMed  Google Scholar 

    12.
    Zera, A. J. The endocrine regulation of wing polymorphism in insects: state of the art, recent surprises, and future directions. Integr. Comp. Biol. 43, 607–616 (2004).
    Google Scholar 

    13.
    Zera, A. J. Evolutionary genetics of juvenile hormone and ecdysteroid regulation in Gryllus: A case study in the microevolution of endocrine regulation. Comp. Biochem. Physiol. A 144, 365–379 (2006).
    Google Scholar 

    14.
    Zera, A. J. Endocrine analysis in evolutionary-developmental studies of insect polymorphism: hormone manipulation versus direct measurement of hormonal regulators. Evol. Dev 9, 499–513 (2007).
    CAS  PubMed  Google Scholar 

    15.
    Hardie, J. Juvenile hormone and photoperiodically controlled polymorphism in Aphis fabae: prenatal effects on presumptive oviparae. J. Insect Physiol. 27, 257–265 (1981).
    CAS  Google Scholar 

    16.
    Hardie, J., Honda, K., Timar, T. & Varjas, L. Effects of 2, 2-dimethylchromene derivatives on wing determination and metamorphosis in the pea aphid, Acyrthosiphon pisum. Arch. Insect Biochem. Physiol. 30, 25–40 (1995).
    CAS  Google Scholar 

    17.
    Ayoade, O., Morooka, S. & Tojo, S. Enhancement of short wing formation and ovarian growth in the genetically defined macropterous strain of the brown planthopper, Nilaparvata lugens. J. Insect Physiol. 45, 93–100 (1999).
    CAS  PubMed  Google Scholar 

    18.
    Sun, B. B. et al. Methoprene influences reproduction and flight capacity in adults of the rice leaf roller, Cnaphalocrocis Medinalis (Guenée) (Lepidoptera: Pyralidae). Arch. Insect Biochem. Physiol. 82(1), 1–13 (2013).
    CAS  PubMed  Google Scholar 

    19.
    Tanaka, S. Endocrine control of ovarian development and flight muscle histolysis in a wing dimorphic cricket, Modicogryllus confirmatus. J. Insect Physiol. 40, 483–490 (1994).
    CAS  Google Scholar 

    20.
    Zera, A. J. & Cisper, G. Genetic and diurnal variation in the juvenile hormone titer in a wing-polymorphic cricket: implications for the evolution of life histories and dispersal. Physiol. Biochem. Zool. 74, 293–306 (2001).
    CAS  PubMed  Google Scholar 

    21.
    Socha, R. & Kula, J. Differential allocation of protein resources to flight muscles and reproductive organs in the flightless wing-polymorphic bug, Pyrrhocoris apterus (L.) (Heteroptera). J. Comp. Physiol. B. 178, 179–188 (2008).
    CAS  PubMed  Google Scholar 

    22.
    Lu, K. et al. Nutritional signaling regulates vitellogenin synthesis and egg development through juvenile hormone in Nilaparvata lugens (Stål). Int. J. Mol. Sci. 17, 269 (2016).
    Google Scholar 

    23.
    Han, E. N. & Gatehouse, A. G. Effect of temperature and photoperiod on the calling behaviour of a migratory insect, the oriental armyworm Mythimna separata. Physiol. Entomol. 16, 419–427 (1991).
    Google Scholar 

    24.
    Luo, L. Z., Li, G. B., Cao, Y. Z. & Hu, Y. The influence of larval rearing density on flight capacity and fecundity of adult oriental armyworm, Mythimna separata (walker). Acta Entomol. Sin 38, 38–45 (1995).
    Google Scholar 

    25.
    Cao, Y. Z., Luo, L. Z. & Guo, J. Performance of adult reproduction and flight in relation to larval nutrition in the oriental armyworm, Mythimna separate (Walker). Acta Entomol. Sin 39, 105–108 (1996).
    Google Scholar 

    26.
    Jiang, X. F., Luo, L. Z. & Hu, Y. Influences of rearing temperature on flight and reproductive capacity of adult oriental armyworm, Mythimna separata (Walker). Acta Entomol. Sin 20, 288–292 (2000).
    Google Scholar 

    27.
    Jiang, X. F., Luo, L. Z. & Hu, Y. Genetic characteristics of pre-oviposition period in the oriental armyworm Mythimna separata (Walker). Acta Entomol. Sin 25, 68–72 (2005).
    Google Scholar 

    28.
    Jiang, X. F., Luo, L. Z. & Zhang, L. Amplified fragment length polymorphism analysis of the oriental armyworm, Mythimna separata (Walker) geographic and melanic laboratory populations in China. J. Econ. Entomol 100, 1525–1532 (2007).
    CAS  PubMed  Google Scholar 

    29.
    Wang, Y. Z. & Zhang, X. X. Studies on the migratory behaviours of oriental armyworm, Mythimna separata (Walker). Acta Ecol. Sin 21, 772–779 (2001).
    Google Scholar 

    30.
    Zhang, L., Luo, L. Z., Jiang, X. F. & Hu, Y. Influences of starvation on the first day after emergence on ovarian development and flight potential in adults of the oriental armyworm, Mythimna separata (Walker) (Lepidopterea: Noctuidae). Acta Entomol. Sin 49, 895–902 (2006).
    Google Scholar 

    31.
    Zhang, L., Luo, L. Z. & Jiang, X. F. Starvation influences allatotropin gene expression and juvenile hormone titer in the female adult oriental armyworm, Mythimna separata. Arch Insect Biochem. Physiol. 68, 63–70 (2008a).
    CAS  PubMed  Google Scholar 

    32.
    Zhang, L., Jiang, X. F. & Luo, L. Z. Determination of sensitive stage for switching migrant oriental armyworms into residents. Environ. Entomol 37, 1389–1395 (2008b).
    PubMed  Google Scholar 

    33.
    Jiang, X. F. & Luo, L. Z. Comparison of behavioral and physiological characteristics between the emigrant and immigrant populations of the oriental armyworm, Mythimna separata (Walker). Acta Entomol. Sin 48, 61–67 (2005).
    Google Scholar 

    34.
    Jiang, X. F., Luo, L. Z., Zhang, L., Sappington, T. W. & Hu, Y. Regulation of migration in the oriental armyworm, Mythimna separata (Walker) in China: A review integrating environmental, physiological, hormonal, genetic, and molecular factors. Environ. Entomol. 40(3), 516–533 (2011).
    CAS  PubMed  Google Scholar 

    35.
    Li, K. B. et al. Influences of flight on energetic reserves and juvenile hormone synthesis by corpora allata of the oriental armyworm, Mythimna separata (Walker). Acta Entomol. Sin 48, 155–160 (2005).
    CAS  Google Scholar 

    36.
    Luo, L. Z., Li, K. B., Jiang, X. F. & Hu, Y. Regulation of flight capacity and contents of energy substances by methoprene in the moths of oriental armyworm, Mythimna separata. Acta Entomol. Sin 8, 63–72 (2001).
    CAS  Google Scholar 

    37.
    Teal, P. E. A., Gomez-Simuta, Y. & Proveaux, A. T. Mating experience and juvenile hormone enhance sexual signaling and mating in male Caribbean fruit flies. Proc. Natl. Acad. Sci. USA 97, 3708–3712 (2000).
    ADS  CAS  PubMed  Google Scholar 

    38.
    Rafaeli, A., Zakharova, T., Lapsker, Z. & Jurenka, R. A. The identification of an age- and female- specific putative PBAN membrane-receptor protein in pheromone glands of Helicoverpa armigera: possible up-regulation by Juvenile Hormone. Insect Biochem. Mol. Biol. 33, 371–380 (2003).
    CAS  PubMed  Google Scholar 

    39.
    Zera, A. J., Zhao, Z. & Kaliseck, K. Hormones in the field: evolutionary endocrinology of juvenile hormone and ecdysteroids in field populations of the wingdimorphic cricket Gryllus firmus. Physiol. Biochem. Zool. 80, 592–606 (2007).
    CAS  PubMed  Google Scholar 

    40.
    Nijhout, H. F. Development and evolution of adaptive polyphenisms. Evol. Dev. 5, 9–18 (2003).
    PubMed  Google Scholar 

    41.
    Roy, S., Saha, T. T., Zou, Z. & Raikhel, A. S. Regulatory pathways controlling female insect reproduction. Annu. Rev. Entomol. 63, 489–511 (2018).
    CAS  PubMed  Google Scholar 

    42.
    Barbora, K. & Marek, J. Juvenile hormone resistance gene Methoprene-tolerant controls entry into metamorphosis in the beetle Tribolium castaneum. Proc. Natl. Acad. Sci. USA 104, 10488–10493 (2007).
    Google Scholar 

    43.
    Baumann, A., Barry, J., Wang, S., Fujiwara, Y. & Wilson, T. G. Paralogous genes involved in juvenile hormone action in Drosophila melanogaster. Genetics 185, 1327–1336 (2010).
    CAS  PubMed  PubMed Central  Google Scholar 

    44.
    Riddiford, L. M., Truman, J. W., Mirth, C. K. & Shen, Y. C. A role for juvenile hormone in the prepupal development of drosophila melanogaster. Development 137, 1117–1126 (2010).
    CAS  PubMed  PubMed Central  Google Scholar 

    45.
    Abdou, M. A. et al. Drosophila met and gce are partially redundant in transducing juvenile hormone action. Insect Biochem. Mol. Biol. 41, 938–945 (2011).
    CAS  PubMed  Google Scholar 

    46.
    Charles, J. P. et al. Ligand-binding properties of a juvenile hormone receptor, Methoprene-tolerant. Proc. Natl. Acad. Sci. USA 108, 21128–21133 (2011).
    ADS  CAS  PubMed  Google Scholar 

    47.
    Li, M., Mead, E. A. & Zhu, J. Heterodimer of two bHLH-PAS proteins mediates juvenile hormone- induced gene expression. Proc. Natl. Acad. Sci. USA 108, 638–643 (2011).
    ADS  CAS  PubMed  Google Scholar 

    48.
    Bernardo, T. J. & Dubrovsky, E. B. The Drosophila juvenile hormone receptor candidates Methoprene-tolerant (Met) and germ cell-expressed (gce) utilize a conserved LIXXL motif to bind the FTZ-F1 nuclear receptor. J. Biol. Chem. 287, 7821–7833 (2012).
    CAS  PubMed  PubMed Central  Google Scholar 

    49.
    Bernardo, T. J. & Dubrovsky, E. B. Molecular mechanisms of transcription activation by juvenile hormone: a critical role for bHLH-PAS and nuclear receptor proteins. Insects 3, 324–338 (2012).
    PubMed  PubMed Central  Google Scholar 

    50.
    Zhang, Z. L., Xu, J., Sheng, Z., Sui, Y. & Palli, S. R. Steroid receptor co-activator is required for juvenile hormone signal transduction through a bHLH-PAS transcription factor, Methoprene tolerant. J. Biol. Chem. 286, 8437–8447 (2011).
    CAS  PubMed  Google Scholar 

    51.
    Jindra, M., Uhlirova, M., Charles, J. P., Smykal, V. & Hill, R. J. Genetic evidence for function of the bHLH-PAS protein Gce /Met as a juvenile hormone receptor. PLoS. Genet. 11(7), e1005394 (2015).
    PubMed  PubMed Central  Google Scholar 

    52.
    Parthasarathy, R. & Palli, S. R. Molecular analysis of nutritional and hormonal regulation of female reproduction in the red flour beetle. Tribolium castaneum. Insect Biochem. Mol. Biol 41, 294–305 (2011).
    CAS  PubMed  Google Scholar 

    53.
    Guo, W. et al. Juvenile hormone-receptor complex acts on Mcm4 and Mcm7 to promote polyploidy and vitellogenesis in the migratory locust. PLOS Genet. 10, e1004702 (2014).
    PubMed  PubMed Central  Google Scholar 

    54.
    Luo, M. et al. Juvenile hormone differentially regulates two Grp78 genes encoding protein chaperones required for insect fat body cell homeostasis and vitellogenesis. J. Biol. Chem. 292, 8823–34 (2017).
    CAS  PubMed  PubMed Central  Google Scholar 

    55.
    Song, J., Wu, Z., Wang, Z., Deng, S. & Zhou, S. Krüppel-homolog 1 mediates juvenile hormone action to promote vitellogenesis and oocyte maturation in the migratory locust. Insect Biochem. Mol. Biol. 52, 94–101 (2014).
    CAS  PubMed  Google Scholar 

    56.
    Wu, Z., Guo, W., Xie, Y. & Zhou, S. Juvenile hormone activates the transcription of cell-division-cycle 6 (Cdc6) for polyploidy-dependent insect vitellogenesis and oogenesis. J. Biol. Chem. 291, 5418–27 (2016).
    CAS  PubMed  PubMed Central  Google Scholar 

    57.
    Wang, Z., Yang, L., Song, J., Kang, L. & Zhou, S. An isoform of Taiman that contains a PRD-repeat motif is indispensable for transducing the vitellogenic juvenile hormone signal in Locusta migratoria. Insect Biochem. Mol. Biol. 82, 31–40 (2017).
    CAS  PubMed  Google Scholar 

    58.
    Cruz, J., Martin, D., Pascual, N., Maestro, J. L. & Piulachs, M. D. Quantity does matter: juvenile hormone and the onset of vitellogenesis in the German cockroach. Insect Biochem. Mol. Biol. 33, 1219–25 (2003).
    CAS  PubMed  Google Scholar 

    59.
    Gujar, H. & Palli, S. R. Juvenile hormone regulation of female reproduction in the common bed bug, Cimex lectularius. Sci. Rep 6, 35546 (2016).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    60.
    Marchal, E., Hult, E. F., Huang, J., Pang, Z. & Stay, B. Methoprene-tolerant (Met) knockdown in the adult female cockroach, Diploptera punctata, completely inhibits ovarian development. PLOS ONE 9, e106737 (2014).
    ADS  PubMed  PubMed Central  Google Scholar 

    61.
    Luo, L. Z., Jiang, X. F., Li, K. B. & Hu, Y. Influences of flight on reproduction and longevity of the oriental armyworm, Mythimna separata (Walker). Acta Entomol. Sin 42, 150–158 (1999).
    Google Scholar 

    62.
    Luo, L. Z. & Li, G. B. Ultrastructure of the flight muscle of adult oriental armyworm, Mythimna separata (Walker). Acta Entomol. Sin 39(2), 141–148 (1996).
    ADS  Google Scholar 

    63.
    Luo, L. Z. An ultrastructural study on the development of flight muscle in adult oriental armyworm, Mythimna separata (Walker). Acta Entomol. Sin 39(4), 366–374 (1996).
    MathSciNet  Google Scholar 

    64.
    Socha, R. & Šula, J. Flight muscles polymorphism in a flightless bug, Pyrrhocoris apterus (L.): Developmental pattern, biochemical profile and endocrine control. J. Insect Physiol. 52, 231–239 (2006).
    CAS  PubMed  Google Scholar 

    65.
    SAS Institute. SAS/STAT User’s Guide, Release 6.03 Ed. SAS Instisute, Cary, NC. (1988). More

  • in

    Mid and long-term ecological impacts of ski run construction on alpine ecosystems

    1.
    Rixen, C. et al. Winter tourism and climate change in the Alps: an assessment of resource consumption snow reliability and future snowmaking potential. Mt. Res. Dev. 31, 229–236 (2011).
    Google Scholar 
    2.
    Vanat, L. International Report on Snow & Mountain Tourism: Overview of the Key Industry Figures for Ski Resorts, 10th edition (2018).

    3.
    Negro, M. et al. Differential responses of ground dwelling arthropods to ski-piste restoration by hydroseeding. Biodivers. Conserv. 22, 2607–2634 (2013).
    Google Scholar 

    4.
    Körner, C. The Alpine life zone under global change. Gayana Bot. https://doi.org/10.4067/S0717-66432000000100001 (2000).
    Article  Google Scholar 

    5.
    Garcı́a-Llorente, M. et al. What can conservation strategies learn from the ecosystem services approach? Insights from ecosystem assessments in two Spanish protected areas. Biodivers. Conserv. 27, 1575–1597 (2016).

    6.
    Egan, P. A. & Price, M. F. Mountain Ecosystem Services and Climate Change. A Global Overview of Potential Threats and Strategies for Adaptation (UNESCO, Paris, 2017).
    Google Scholar 

    7.
    MeijerzuSchlochtern, M. P., Rixen, C., Wipf, S. & Cornelissen, J. H. C. Management, winter climate and plant–soil feedbacks on ski slopes: a synthesis. Ecol. Res. 29, 583–592 (2014).
    CAS  Google Scholar 

    8.
    Gros, R., Monrozier, L. J., Bartoli, F., Chotte, J. L. & Faivre, P. Relationships between soil physico-chemical properties and microbial activity along a restoration chronosequence of alpine grasslands following ski run construction. Appl. Soil Ecol. 27, 7–22 (2004).
    Google Scholar 

    9.
    Barni, E., Freppaz, M. & Siniscalco, C. Interactions between Vegetation, Roots, and Soil Stability in Restored High-altitude Ski Runs in the Alps. Arct. Antarct. Alp. Res. 39, 25–33 (2007).
    Google Scholar 

    10.
    Pohl, M., Alig, D., Körner, C. & Rixen, C. Higher plant diversity enhances soil stability in disturbed alpine ecosystems. Plant Soil 324, 91–102 (2009).
    CAS  Google Scholar 

    11.
    Burt, J. W. & Rice, K. J. Not all ski slopes are created equal: Disturbance intensity affects ecosystem properties. Ecol. Appl. 19, 2242–2253 (2009).
    PubMed  Google Scholar 

    12.
    Van Andel, J., Bakker, J. P., Bakker, J. P. & Grootjans, A. P. Mechanism of vegetation succession: a review of concepts and perspectives. Acta Bot. Neerlandica 42, 413–433 (1993).
    Google Scholar 

    13.
    Styczen, M. E. & Morgan, R. P. C. Engineering properties of vegetation 5–58 (E and FN Spon, New York, 1995).
    Google Scholar 

    14.
    Gray, D. H. & Sotir, R. B. Biotechnical and Soil Bioengineering Slope Stabilization: A Practical Guide for Erosion Control (Wiley, New York, 1996).
    Google Scholar 

    15.
    Gray, D. H. & Leiser, A. T. Biotechnical Slope Protection and Erosion Control (Van Nostrand Reinhold Company, London, 1982).
    Google Scholar 

    16.
    Argenti, G. & Ferrari, L. Plant cover evolution and naturalisation of revegetated ski runs in an Apennine ski resort (Italy). Forest 2, 178–182 (2009).
    Google Scholar 

    17.
    Pintaldi, E. et al. Hummocks affect soil properties and soil-vegetation relationships in a subalpine grassland (North-Western Italian Alps). CATENA 145, 214–226 (2016).
    Google Scholar 

    18.
    Stokes, A. et al. Ecological mitigation of hillslope instability: ten key issues facing researchers and practitioners. Plant Soil 377, 1 (2014).
    CAS  Google Scholar 

    19.
    Burt, J. W. & Clary, J. J. Initial disturbance intensity affects recovery rates and successional divergence on abandoned ski slopes. J. Appl. Ecol. 53, 607–615 (2016).
    Google Scholar 

    20.
    Krautzer, B. et al. The influence of recultivation technique and seed mixture on erosion stability after restoration in mountain environment. Nat. Haz. 56, 547–557 (2011).
    Google Scholar 

    21.
    Pintaldi, E. et al. Sustainable soil management in ski areas: threats and challenges. Sustainability 9, 2150 (2017).
    Google Scholar 

    22.
    Pohl, M., Stroude, R., Buttler, A. & Rixen, C. Functional traits and root morphology of alpine plants. Ann. Bot. 108, 537–545 (2011).
    PubMed  PubMed Central  Google Scholar 

    23.
    Körner, C. Alpine Plant Life Functional Plant Ecology of High Mountain Ecosystems (Springer-Verlag, Berlin, 2003).
    Google Scholar 

    24.
    Mercalli, L. Atlante climatico della Valle d’Aosta (Società Meteorologica Italiana, Rome, 2003).
    Google Scholar 

    25.
    FAO-ISRIC. World Reference Base for Soil Resources 2014. World Soil Resources Reports No. 103 (FAO, 2014).

    26.
    Shannon, C. E. & Wiener, W. The Mathematical Theory of Communication (University Illinois Press, Champaign, 1963).
    Google Scholar 

    27.
    Van Andel, J. & Aronson, J. Restoration Ecology. The New Frontier 2nd edn. (Wiley-Blackwell, New York, 2012).
    Google Scholar 

    28.
    Landolt, E. et al. Flora Indicativa: Okologische Zeigerwerte und Biologische Kennzeichen zur Flora der Schweiz und der Alpen (Haupt, Bern, 2010).
    Google Scholar 

    29.
    Bovio, M. Lista Rossa e Lista Nera della flora vascolare della Valle d’Aosta (Italia, Alpi Nord-occidentali). Aggiornamento anno 2016. Rev. Valdôtaine Hist. Nat. 70, 57–74 (2016).
    Google Scholar 

    30.
    Rossi, G. et al. Lista Rossa della Flora Italiana. 1. Policy Species e Altre Specie Minacciate (Comitato Italiano IUCN e Ministero dell’Ambiente e della Tutela del Territorio e del Mare, Rome, 2013).
    Google Scholar 

    31.
    Aeschimann, P., Lauber, K., Moser, D. M. & Theurillat, J. P. Flora Alpina (Haupt Verlag, Bern, 2004).
    Google Scholar 

    32.
    Van Reeuwijk, L. P. Procedures for Soil Analysis. Technical Paper n. 9 (International Soil Reference and Information Centre, Wageningen, 2002).

    33.
    Zanini, E., Bonifacio, E., Alberston, J. D. & Nielsen, D. R. Topsoil aggregate breakdown under water-saturated conditions. Soil. Sci. 163, 288–298 (1998).
    ADS  CAS  Google Scholar 

    34.
    Kruskal, J. B. Nonmetric multidimensional scaling: a numerical method. Psychometrika 29, 115–129 (1964).
    MATH  MathSciNet  Google Scholar 

    35.
    Oksanen, J. et al. Vegan: community ecology package. R Package Version 2.0-0. ttp://CRAN.Rproject.org/package=vegan (2011).

    36.
    Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
    Google Scholar 

    37.
    Wipf, S., Rixen, C., Fischer, M., Schmid, B. & Stoeckli, V. Effects of ski piste preparation on alpine vegetation. J. Appl. Ecol. 42, 306–316 (2005).
    Google Scholar 

    38.
    Roux-Fouillet, P., Wipf, S. & Rixen, C. Long-term impacts of ski piste management on alpine vegetation and soils. J. Appl. Ecol. 48, 906–915 (2011).
    Google Scholar 

    39.
    Delgado, R. et al. Impact of ski pistes on soil properties, a case study from a mountainous area in the Mediterranean region. Soil Use Manag. 23, 269–277 (2007).
    Google Scholar 

    40.
    Argenti, G., Merati, M., Staglianò, N. & Talamucci, P. Establishment and evolution of technical ski slope covers in an alpine environment. Riv. Agron. 34, 186–190 (2000).
    Google Scholar 

    41.
    Krautzer, B. et al. Site-specific high zone restoration in the Alpine region: the current technological development (HBLFA Raumberg-Gumpenstein, Irdning, 2006).
    Google Scholar 

    42.
    Burt, J. W. Developing restoration planting mixes for active ski slopes: a multi-site reference community approach. J. Environ. Manage. 49, 636–648 (2012).
    ADS  Google Scholar 

    43.
    Klug, B. Seed mixtures, seeding methods, and soil seed pools: major factors in erosion control on graded ski-runs. WSEAS Trans. Environ. Dev. 4, 454–459 (2006).
    Google Scholar 

    44.
    Barrel, A. et al. Native Seeds for the Ecological Restoration in Mountain Zone: Production and Use of Preservation Mixtures (Institut Agricole Régional, Aosta, 2015).
    Google Scholar 

    45.
    Hagen, D., Hansen, T.-I., Graae, B. J. & Rydgren, K. To seed or not to seed in alpine restoration: introduced grass species outcompete rather than facilitate native species. Ecol. Eng. 64, 255–261 (2014).
    Google Scholar 

    46.
    Gretarsdottir, J., Aradottir, A. L., Vandvik, V., Heegaard, E. & Birks, H. J. B. Long-term effects of reclamation treatments on plant succession in Iceland. Restor. Ecol. 12, 268–278 (2004).
    Google Scholar 

    47.
    Florineth, F. Pflanzen statt Beton (Handbuch zur Ingenieurbiologie und Vegetationstechnik, Berlin-Hannover, 2004).
    Google Scholar 

    48.
    Lichtenegger, E. Root distribution in some alpine plants. Acta Phytogeogr Suec. 81, 76–82 (1996).
    Google Scholar 

    49.
    Nagelmüller, S., Hiltbrunner, E. & Körner, C. Critically low soil temperatures for root growth and root morphology in three alpine plant species. Alp. Bot. 126, 11–21 (2016).
    Google Scholar 

    50.
    Khan, M. A., Gemenet, D. C. & Villordon, A. Root system architecture and abiotic stress tolerance: current knowledge in root and tuber crops. Front. Plant Sci. 7, 1584 (2016).
    CAS  PubMed  PubMed Central  Google Scholar 

    51.
    Tracy, S. R. et al. Quantifying the impact of soil compaction on root system architecture in tomato (Solanum lycopersicum) by X-ray micro-computed tomography. Ann. Bot. 110, 511–519 (2012).
    PubMed  PubMed Central  Google Scholar 

    52.
    Poorter, H. et al. Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol. 193, 30–50 (2012).
    CAS  PubMed  Google Scholar 

    53.
    Bardgett, R. D., Mommer, L. & De Vries, F. T. Going underground: root traits as drivers of ecosystem processes. Trends Ecol. Evol. 29, 692–699 (2014).
    PubMed  Google Scholar 

    54.
    Hudek, C., Stanchi, S., D’Amico, M. & Freppaz, M. Quantifying the contribution of the root system of alpine vegetation in the soil aggregate stability of moraine. Int. Soil Water Conserv. Res. 5, 36–42 (2017).
    Google Scholar 

    55.
    Gould, I. J., Quinton, J. N., Weigelt, A., De Deyn, G. B. & Bardgett, R. D. Plant diversity and root traits benefit physical properties key to soil function in grasslands. Ecol. Lett. 19, 1140–1149 (2016).
    PubMed  PubMed Central  Google Scholar 

    56.
    Solly, E. F. et al. Unravelling the age of fine roots of temperate and boreal forests. Nat. Commun. 9, 3006 (2018).
    ADS  PubMed  PubMed Central  Google Scholar 

    57.
    Rixen, C., Freppaz, M., Stöckli, V., Huovinen, C. & Wipf, S. Altered snow density and chemistry change soil nitrogen mineralization and plant growth. Arct. Antarct. Alp. Res. 40, 568–575 (2008).
    Google Scholar 

    58.
    Miransari, M. Plant growth promoting Rhizobacteria. J. Plant Nutr. 37, 2227–2235 (2014).
    CAS  Google Scholar 

    59.
    Stokes, A., Atger, C., Bengough, A. G., Fourcaud, T. & Sidle, R. C. Desirable plant root traits for protecting natural and engineered slopes against landslides. Plant Soil 324, 1–30 (2009).
    CAS  Google Scholar 

    60.
    Freppaz, M. et al. Soil Properties on Ski-Runs. In Impacts of Skiing and Related Winter Recreational Activities on Mountain Environments p (eds Rixen, C. & Rolando, A.) 45–64 (Bentham Science Publisher, Sharjah, 2013).
    Google Scholar 

    61.
    Locher Oberholzer, N. et al. Linee Guida per Il Rinverdimento ad Alta Quota; AGHB Bollettino n2 (Luglio, Verein für Ingenieurbiologie, 2008) ((In Italian)).
    Google Scholar 

    62.
    Graf, F. & Brunner, I. Natural and synthesized ectomycorrhizas of the alpine dwarf willow Salix herbacea. Mycorrhiza 6, 227–235 (1996).
    Google Scholar 

    63.
    Graf, F. Ectomycorrhiza in alpine eco-engineering. Rev. Valdôtaine Hist. Nat. 52, 314–323 (1997).
    MathSciNet  Google Scholar 

    64.
    Graf, F. & Gerber, W. Der Einfluss von Mykorrhizapilzen auf die Bodenstruktur und deren Bedeutung für den Lebendverbau Schweiz. Z. Forstwes 11, 863–886 (1997).
    Google Scholar 

    65.
    Frei, M. et al. Quantification of the influence of vegetation on soil stability. In Proceeding of the International Conference on Slope Engineering (Department of Civil Engineering, 2003).

    66.
    Krautzer, B., Graiss, W. & Klug, B. Ecological Restoration of Ski-Runs. The Impacts of Skiing and Related Winter Recreational Activities on Mountain Environments 184–209 (Bentham e books, Sharjah, 2013).
    Google Scholar 

    67.
    Peratoner, G. Organic Seed Propagation of Alpine Species and Their Use in Ecological Restoration of Ski-Runs in Mountain Regions. Diss. Univ. Kassel. Kassel University Press, 238 (2003). More

  • in

    Increased temperature has no consequence for behavioral manipulation despite effects on both partners in the interaction between a crustacean host and a manipulative parasite

    1.
    Deguines, N., Brashares, J. S. & Prugh, L. R. Precipitation alters interactions in a grassland ecological community. J. Anim. Ecol. 86, 262–272 (2017).
    PubMed  Google Scholar 
    2.
    Bernabé, T. N. et al. Warming weakens facilitative interactions between decomposers and detritivores, and modifies freshwater ecosystem functioning. Glob. Change Biol. 24, 3170–3186 (2018).
    ADS  Google Scholar 

    3.
    Boulangeat, I., Svenning, J. C., Daufresne, T., Leblond, M. & Gravel, D. The transient response of ecosystems to climate change is amplified by trophic interactions. Oikos 127, 1822–1833 (2018).
    Google Scholar 

    4.
    Salt, J. L., Bulit, C., Zhang, W., Qi, H. & Montagnes, D. J. S. Spatial extinction or persistence: Landscape–temperature interactions perturb predator–prey dynamics. Ecography (Cop.) 40, 1177–1186 (2017).
    Google Scholar 

    5.
    Zhang, L., Takahashi, D., Hartvig, M. & Andersen, K. H. Food-web dynamics under climate change. Proc. R. Soc. B 284, 20171772 (2017).
    PubMed  Google Scholar 

    6.
    Campanati, C., Dupont, S., Williams, G. A. & Thiyagarajan, V. Differential sensitivity of larvae to ocean acidification in two interacting mollusc species. Mar. Environ. Res. 141, 66–74 (2018).
    CAS  PubMed  Google Scholar 

    7.
    Woehler, E., Patterson, T. A., Bravington, M. V., Hobday, A. J. & Chambers, L. E. Climate and competition in abundance trends in native and invasive Tasmanian gulls. Mar. Ecol. Prog. Ser. 511, 249–263 (2014).
    ADS  Google Scholar 

    8.
    Frizzi, F., Bartalesi, V. & Santini, G. Combined effects of temperature and interspecific competition on the mortality of the invasive garden ant, Lasius neglectus: A laboratory study. J. Therm. Biol. 65, 76–81 (2017).
    PubMed  Google Scholar 

    9.
    Grainger, T. N., Rego, A. I. & Gilbert, B. Temperature-dependent species interactions shape priority effects and the persistence of unequal competitors. Am. Nat. 191, 197–209 (2018).
    PubMed  Google Scholar 

    10.
    Friesen, O. C., Poulin, R. & Lagrue, C. Parasite-mediated microhabitat segregation between congeneric hosts. Biol. Lett. 14, 20170671 (2018).
    PubMed  PubMed Central  Google Scholar 

    11.
    Srinivasan, U., Elsen, P. R., Tingley, M. W. & Wilcove, D. S. Temperature and competition interact to structure Himalayan bird communities. Proc. R. Soc. B Biol. Sci. 285, 20172593 (2018).
    Google Scholar 

    12.
    Franke, F., Armitage, S. A. O., Kutzer, M. A. M., Kurtz, J. & Scharsack, J. P. Environmental temperature variation influences fitness trade-offs and tolerance in a fish–tapeworm association. Parasit. Vectors 10, 252 (2017).
    PubMed  PubMed Central  Google Scholar 

    13.
    Castano-Vazquez, F., Martinez, J., Merino, S. & Lozano, M. Experimental manipulation of temperature reduce ectoparasites in nests of blue tits Cyanistes caeruleus. J. Avian Biol. 49, UNSP e01695 (2018).
    Google Scholar 

    14.
    Paull, S. H. & Johnson, P. T. J. How temperature, pond-drying, and nutrients influence parasite infection and pathology. EcoHealth 15, 396–408 (2018).
    PubMed  PubMed Central  Google Scholar 

    15.
    Larsen, M. H. & Mouritsen, K. N. Temperature–parasitism synergy alters intertidal soft-bottom community structure. J. Exp. Mar. Bio. Ecol. 460, 109–119 (2014).
    Google Scholar 

    16.
    Marcogliese, D. J. The distribution and abundance of parasites in aquatic ecosystems in a changing climate: More than just temperature. Integr. Comp. Biol. 56, 611–619 (2016).
    PubMed  Google Scholar 

    17.
    Mouritsen, K. N., Sørensen, M. M., Poulin, R. & Fredensborg, B. L. Coastal ecosystems on a tipping point: Global warming and parasitism combine to alter community structure and function. Glob. Change Biol. 24, 4340–4356 (2018).
    ADS  Google Scholar 

    18.
    Hatcher, M. J., Dick, J. T. A. & Dunn, A. M. Diverse effects of parasites in ecosystems: Linking interdependent processes. Front. Ecol. Environ. 10, 186–194 (2012).
    Google Scholar 

    19.
    Repetto, M. & Griffen, B. D. Physiological consequences of parasite infection in the burrowing mud shrimp, Upogebia pugettensis, a widespread ecosystem engineer. Mar. Freshw. Res. 63, 60–67 (2012).
    Google Scholar 

    20.
    Boze, B. G. V. & Moore, J. The effect of a nematode parasite on feeding and dung-burying behavior of an ecosystem engineer. Integr. Comp. Biol. 54, 177–183 (2014).
    CAS  PubMed  Google Scholar 

    21.
    Laverty, C. et al. Temperature rise and parasitic infection interact to increase the impact of an invasive species. Int. J. Parasitol. 47, 291–296 (2017).
    PubMed  Google Scholar 

    22.
    Labaude, S., Cézilly, F. & Rigaud, T. Temperature-related intraspecific variability in the behavioral manipulation of acanthocephalan parasites on their gammarid hosts. Biol. Bull. 232, 82–90 (2017).

    23.
    Labaude, S., Rigaud, T. & Cézilly, F. Additive effects of temperature and infection with an acanthocephalan parasite on the shredding activity of Gammarus fossarum (Crustacea: Amphipoda): The importance of aggregative behavior. Glob. Chang. Biol. 23, 1415–1424 (2017).

    24.
    MacNeil, C., Dick, J. T. A. & Elwood, R. W. The trophic ecology of freshwater Gammarus spp. (crustacea:amphipoda): Problems and perspectives concerning the functional feeding group concept. Biol. Rev. 72, 349–364 (1997).
    Google Scholar 

    25.
    Piscart, C., Genoel, R., Doledec, S., Chauvet, E. & Marmonier, P. Effects of intense agricultural practices on heterotrophic processes in streams. Environ. Pollut. 157, 1011–1018 (2009).
    CAS  PubMed  Google Scholar 

    26.
    Degani, G., Bromley, H. J., Ortal, R., Netzer, Y. & Harari, N. Diets of rainbow trout (Salmo gairdneri) in a thermally constant stream. Vie Milieu 37, 99–103 (1987).
    Google Scholar 

    27.
    Friberg, N. et al. The effect of brown trout (Salmo trutta L.) on stream invertebrate drift, with special reference to Gammarus pulex L. Hydrobiologia 294, 105–110 (1994).
    Google Scholar 

    28.
    Kelly, D. W., Dick, J. T. A. & Montgomery, W. I. The functional role of Gammarus (Crustacea, Amphipoda): Shredders, predators, or both?. Hydrobiologia 485, 199–203 (2002).
    Google Scholar 

    29.
    Piscart, C., Bergerot, B., Laffaille, P. & Marmonier, P. Are amphipod invaders a threat to regional biodiversity?. Biol. Invasions 12, 853–863 (2010).
    Google Scholar 

    30.
    Constable, D. & Birkby, N. J. The impact of the invasive amphipod Dikerogammarus haemobaphes on leaf litter processing in UK rivers. Aquat. Ecol. 50, 273–281 (2016).
    Google Scholar 

    31.
    Foucreau, N., Puijalon, S., Hervant, F. & Piscart, C. Effect of leaf litter characteristics on leaf conditioning and on consumption by Gammarus pulex. Freshw. Biol. 58, 1672–1681 (2013).
    Google Scholar 

    32.
    Maltby, L., Clayton, S. A., Wood, R. M. & McLoughlin, N. Evaluation of the Gammarus pulex in situ feeding assay as a biomonitor of water quality: Robustness, responsiveness, and relevance. Environ. Toxicol. Chem. 21, 361–368 (2002).
    CAS  PubMed  Google Scholar 

    33.
    Benesh, D. P., Lafferty, K. D. & Kuris, A. A life cycle database for parasitic acanthocephalans, cestodes, and nematodes. Ecology 98, 882–882 (2017).
    PubMed  Google Scholar 

    34.
    Crompton, D. W. T. & Nickol, B. B. Biology of the Acanthocephala (Cambridge University Press, Cambridge, 1985).
    Google Scholar 

    35.
    Bakker, T. C. M., Frommen, J. G. & Thünken, T. Adaptive parasitic manipulation as exemplified by acanthocephalans. Ethology https://doi.org/10.1111/eth.12660 (2017).
    Article  Google Scholar 

    36.
    Bethel, W. M. & Holmes, J. C. Altered evasive behavior and responses to light in amphipods harboring acanthocephalan cystacanths. J. Parasitol. 59, 945–956 (1973).
    Google Scholar 

    37.
    Bauer, A., Trouvé, S., Grégoire, A., Bollache, L. & Cézilly, F. Differential influence of Pomphorhynchus laevis (Acanthocephala) on the behaviour of native and invader gammarid species. Int. J. Parasitol. 30, 1453–1457 (2000).
    CAS  PubMed  Google Scholar 

    38.
    Kaldonski, N., Perrot-Minnot, M.-J. & Cézilly, F. Differential influence of two acanthocephalan parasites on the antipredator behaviour of their common intermediate host. Anim. Behav. 74, 1311–1317 (2007).
    Google Scholar 

    39.
    McCahon, C. P., Brown, A. F. & Pascoe, D. The effect of the acanthocephalan Pomphorhynchus laevis (Müller 1776) on the acute toxicity of cadmium to its intermediate host, the amphipod Gammarus pulex (L.). Arch. Environ. Contam. Toxicol. 17, 239–243 (1988).
    CAS  Google Scholar 

    40.
    Médoc, V., Piscart, C., Maazouzi, C., Simon, L. & Beisel, J.-N. Parasite-induced changes in the diet of a freshwater amphipod: Field and laboratory evidence. Parasitology 138, 537–546 (2011).
    PubMed  Google Scholar 

    41.
    Cornet, S., Franceschi, N., Bauer, A., Rigaud, T. & Moret, Y. Immune depression induced by acanthocephalan parasites in their intermediate crustacean host: Consequences for the risk of super-infection and links with host behavioural manipulation. Int. J. Parasitol. 39, 221–229 (2009).
    CAS  PubMed  Google Scholar 

    42.
    Plaistow, S. J., Troussard, J.-P. & Cézilly, F. The effect of the acanthocephalan parasite Pomphorhynchus laevis on the lipid and glycogen content of its intermediate host Gammarus pulex. Int. J. Parasitol. 31, 346–351 (2001).
    CAS  PubMed  Google Scholar 

    43.
    Bollache, L., Rigaud, T. & Cézilly, F. Effects of two acanthocephalan parasites on the fecundity and pairing status of female Gammarus pulex (Crustacea: Amphipoda). J. Invertebr. Pathol. 79, 102–110 (2002).
    CAS  PubMed  Google Scholar 

    44.
    Dezfuli, B. S., Lui, A., Giovinazzo, G. & Giari, L. Effect of Acanthocephala infection on the reproductive potential of crustacean intermediate hosts. J. Invertebr. Pathol. 98, 116–119 (2008).
    CAS  PubMed  Google Scholar 

    45.
    Labaude, S., Cézilly, F., Tercier, X. & Rigaud, T. Influence of host nutritional condition on post-infection traits in the association between the manipulative acanthocephalan Pomphorhynchus laevis and the amphipod Gammarus pulex. Parasit. Vectors 8, 403 (2015).
    PubMed  PubMed Central  Google Scholar 

    46.
    Rumpus, A. E. & Kennedy, C. R. The effect of the acanthocephalan Pomphorhynchus laevis upon the respiration of its intermediate host, Gammarus pulex. Parasitology 68, 271–284 (1974).
    CAS  PubMed  Google Scholar 

    47.
    Perrot-Minnot, M.-J., Kaldonski, N. & Cézilly, F. Increased susceptibility to predation and altered anti-predator behaviour in an acanthocephalan-infected amphipod. Int. J. Parasitol. 37, 645–651 (2007).
    PubMed  Google Scholar 

    48.
    Hindsbo, O. Effects of Polymorphus (Acanthocephala) on colour and behaviour of Gammarus lacustris. Nature 238, 333 (1972).
    ADS  Google Scholar 

    49.
    Dianne, L. et al. Protection first then facilitation: A manipulative parasite modulates the vulnerability to predation of its intermediate host according to its own developmental stage. Evolution 65, 2692–2698 (2011).
    PubMed  Google Scholar 

    50.
    Lagrue, C., Kaldonski, N., Perrot-Minnot, M.-J., Motreuil, S. & Bollache, L. Modification of hosts’ behavior by a parasite: Field evidence for adaptive manipulation. Ecology 88, 2839–2847 (2007).
    PubMed  Google Scholar 

    51.
    Kaldonski, N., Perrot-Minnot, M.-J., Motreuil, S. & Cézilly, F. Infection with acanthocephalans increases the vulnerability of Gammarus pulex (Crustacea Amphipoda) to non-host invertebrate predators. Parasitology 135, 627–632 (2008).
    CAS  PubMed  Google Scholar 

    52.
    Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. B. & Charnov, E. L. Effects of size and temperature on metabolic rate. Science 293, 2248–2251 (2001).
    ADS  CAS  PubMed  Google Scholar 

    53.
    Roux, C. & Roux, A. L. Température et métabolisme respiratoire d’espèces sympatriques de gammares du groupe pulex (Crustacés, Amphipodes). Ann. Limnol. 3, 3–16 (1967).
    Google Scholar 

    54.
    Issartel, J., Hervant, F., Voituron, Y., Renault, D. & Vernon, P. Behavioural, ventilatory and respiratory responses of epigean and hypogean crustaceans to different temperatures. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 141, 1–7 (2005).
    PubMed  Google Scholar 

    55.
    Foucreau, N., Cottin, D., Piscart, C. & Hervant, F. Physiological and metabolic responses to rising temperature in Gammarus pulex (Crustacea) populations living under continental or Mediterranean climates. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 168, 69–75 (2014).
    CAS  PubMed  Google Scholar 

    56.
    Moenickes, S. et al. From population-level effects to individual response: Modelling temperature dependence in Gammarus pulex. J. Exp. Biol. 214, 3678–3687 (2011).
    PubMed  Google Scholar 

    57.
    Barber, I., Berkhout, B. W. & Ismail, Z. Thermal change and the dynamics of multi-host parasite life cycles in aquatic ecosystems. Integr. Comp. Biol. 56, 561–572 (2016).
    PubMed  PubMed Central  Google Scholar 

    58.
    Olson, R. E. & Pratt, I. The life cycle and larval development of Echinorhynchus lageniformis Ekbaum, 1938 (Acanthocephala: Echinorhynchidae). J. Parasitol. 57, 143–149 (1971).
    Google Scholar 

    59.
    Tokeson, J. P. E. & Holmes, J. C. The effects of temperature and oxygen on the development of Polymorphus marilis (Acanthocephala) in Gammarus lacustris (Amphipoda). J. Parasitol. 68, 112–119 (1982).
    Google Scholar 

    60.
    Sheath, D. J., Andreou, D. & Britton, J. R. Interactions of warming and exposure affect susceptibility to parasite infection in a temperate fish species. Parasitology 143, 1340–1346 (2016).
    PubMed  Google Scholar 

    61.
    VanCleave, H. J. Seasonal distribution of some acanthocephala from fresh-water hosts. J. Parasitol. 2, 106–110 (1916).
    Google Scholar 

    62.
    Muzzall, P. M. & Rabalais, F. C. Studies on Acanthocephalus jacksoni Bullock, 1962 (Acanthocephala: Echinorhynchidae). I. Seasonal periodicity and new host records. Proc. Helminthol. Soc. Wash. 42, 31–34 (1975).
    Google Scholar 

    63.
    Brown, A. F. Seasonal dynamics of the acanthocephalan Pomphorhynchus laevis (Muller, 1776) in its intermediate and preferred definitive hosts. J. Fish Biol. 34, 183–194 (1989).
    Google Scholar 

    64.
    Rauque, C. A. & Semenas, L. Infection pattern of two sympatric acanthocephalan species in the amphipod Hyalella patagonica (Amphipoda: Hyalellidae) from Lake Mascardi (Patagonia, Argentina). Parasitol. Res. 100, 1271–1276 (2007).
    PubMed  Google Scholar 

    65.
    Wali, A. et al. Distribution of helminth parasites in intestines and their seasonal rate of infestation in three freshwater fishes of Kashmir. J. Parasitol. Res. https://doi.org/10.1155/2016/8901518 (2016).
    Article  PubMed  PubMed Central  Google Scholar 

    66.
    Guinnee, M. A. & Moore, J. The effect of parasitism on host fecundity is dependent on temperature in a cockroach-acanthocephalan system. J. Parasitol. 90, 673–677 (2004).
    PubMed  Google Scholar 

    67.
    Benesh, D. P., Hasu, T., Seppälä, O. & Valtonen, E. T. Seasonal changes in host phenotype manipulation by an acanthocephalan: Time to be transmitted?. Parasitology 136, 219–230 (2009).
    CAS  PubMed  Google Scholar 

    68.
    Perrot-Minnot, M.-J., Maddaleno, M., Balourdet, A. & Cézilly, F. Host manipulation revisited: No evidence for a causal link between altered photophobia and increased trophic transmission of amphipods infected with acanthocephalans. Funct. Ecol. 26, 1007–1014 (2012).
    Google Scholar 

    69.
    Benesh, D. P., Duclos, L. M. & Nickol, B. B. The behavioral response of amphipods harboring Corynosoma constrictum (Acanthocephala) to various components of light. J. Parasitol. 91, 731–736 (2005).
    PubMed  Google Scholar 

    70.
    Dianne, L., Bollache, L., Lagrue, C., Franceschi, N. & Rigaud, T. Larval size in acanthocephalan parasites: Influence of intraspecific competition and effects on intermediate host behavioural changes. Parasit. Vectors 5, 166 (2012).
    PubMed  PubMed Central  Google Scholar 

    71.
    Franceschi, N. et al. Co-variation between the intensity of behavioural manipulation and parasite development time in an acanthocephalan–amphipod system. J. Evol. Biol. 23, 2143–2150 (2010).
    CAS  PubMed  Google Scholar 

    72.
    Perrot-Minnot, M.-J., Sanchez-Thirion, K. & Cézilly, F. Multidimensionality in host manipulation mimicked by serotonin injection. Proc. R. Soc. B Biol. Sci. 281, 20141915 (2014).
    Google Scholar 

    73.
    Franceschi, N., Bauer, A., Bollache, L. & Rigaud, T. The effects of parasite age and intensity on variability in acanthocephalan-induced behavioural manipulation. Int. J. Parasitol. 38, 1161–1170 (2008).
    CAS  PubMed  Google Scholar 

    74.
    Franceschi, N. et al. Variation between populations and local adaptation in acanthocephalan-induced parasite manipulation. Evolution 64, 2417–2430 (2010).
    PubMed  Google Scholar 

    75.
    Cézilly, F., Grégoire, A. & Bertin, A. Conflict between co-occuring manipulative parasites; an experimental study of the joint influence of two acanthocephalan parasites on the behaviour of Gammarus pulex. Parasitology 120, 625–630 (2000).
    PubMed  Google Scholar 

    76.
    Bauer, A., Haine, E. R., Perrot-Minnot, M.-J. & Rigaud, T. The acanthocephalan parasite Polymorphus minutus alters the geotactic and clinging behaviours of two sympatric amphipod hosts: the native Gammarus pulex and the invasive Gammarus roeseli. J. Zool. 267, 39–43 (2005).
    Google Scholar 

    77.
    Xu, Y., Castel, T., Richard, Y., Cuccia, C. & Bois, B. Burgundy regional climate change and its potential impact on grapevines. Clim. Dyn. 39, 1613–1626 (2012).
    Google Scholar 

    78.
    Gunn, J. & Crumley, C. L. Global energy balance and regional hydrology: A Burgundian case study. Earth Surf. Process. Landforms 16, 579–592 (1991).
    ADS  Google Scholar 

    79.
    Rowell, D. P. A scenario of European climate change for the late twenty-first century: Seasonal means and interannual variability. Clim. Dyn. 25, 837–849 (2005).
    Google Scholar 

    80.
    Bollache, L., Gambade, G. & Cézilly, F. The influence of micro-habitat segregation on size assortative pairing in Gammarus pulex (L.) (Crustacea, Amphipoda). Arch. für Hydrobiol. 147, 547–558 (2000).
    Google Scholar 

    81.
    Dezfuli, B. S., Zanini, N., Reggiani, G. & Rossi, R. Echinogammarus stammen (Amphipoda) as an intermediate host for Pomphorhynchus laevis (Acanthocephala) parasite of fishes from the river Brenta. Bolletino di Zool. 58, 267–271 (1991).
    Google Scholar 

    82.
    Dianne, L., Perrot-Minnot, M.-J., Bauer, A., Guvenatam, A. & Rigaud, T. Parasite-induced alteration of plastic response to predation threat: increased refuge use but lower food intake in Gammarus pulex infected with the acanothocephalan Pomphorhynchus laevis. Int. J. Parasitol. 44, 211–216 (2014).
    PubMed  Google Scholar 

    83.
    Hammond, B. A. the proboscis mechanism of Acanthocephalus ranae. J. Exp. Biol. 45, 203–213 (1966).
    Google Scholar 

    84.
    Taraschewski, H. Host–parasite interactions in Acanthocephala: A morphological approach. Adv. Parasitol. 46, 1–179 (2000).
    CAS  PubMed  Google Scholar 

    85.
    Perrot-Minnot, M.-J., Gaillard, M., Dodet, R. & Cézilly, F. Interspecific differences in carotenoid content and sensitivity to UVB radiation in three acanthocephalan parasites exploiting a common intermediate host. Int. J. Parasitol. 41, 173–181 (2011).
    CAS  PubMed  Google Scholar 

    86.
    Kennedy, C. R., Broughton, P. F. & Hine, P. M. The status of brown and rainbow trout, Salmo trutta and S. gairdneri as hosts of the acanthocephalan, Pomphorhynchus laevis. J. Fish Biol. 13, 265–275 (1978).
    Google Scholar 

    87.
    Foucreau, N., Piscart, C., Puijalon, S. & Hervant, F. Effects of rising temperature on a functional process: Consumption and digestion of leaf litter by a freshwater shredder. Fundam. Appl. Limnol./Arch. für Hydrobiol. 187, 295–306 (2016).
    Google Scholar 

    88.
    Noguchi, K., Gel, Y. R., Brunner, E. & Konietschke, F. nparLD: An R software package for the nonparametric analysis of longitudinal data in factorial experiments. J. Stat. Softw. 50, 1–23 (2012).
    Google Scholar 

    89.
    Pellan, L., Médoc, V., Renault, D., Spataro, T. & Piscart, C. Feeding choice and predation pressure of two invasive gammarids, Gammarus tigrinus and Dikerogammarus villosus, under increasing temperature. Hydrobiologia 781, 43–54 (2015).
    Google Scholar 

    90.
    Maure, F. et al. The cost of a bodyguard. Biol. Lett. 7, 843–846 (2011).
    PubMed  PubMed Central  Google Scholar 

    91.
    Maazouzi, C., Piscart, C., Legier, F. & Hervant, F. Ecophysiological responses to temperature of the ‘killer shrimp’ Dikerogammarus villosus: Is the invader really stronger than the native Gammarus pulex?. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 159, 268–274 (2011).
    CAS  PubMed  Google Scholar 

    92.
    Maynard, B. J., Wellnitz, T. A., Zanini, N., Wright, W. G. & Dezfuli, B. S. Parasite-altered behavior in a crustacean intermediate host: Field and laboratory studies. J. Parasitol. 84, 1102–1106 (1998).
    CAS  PubMed  Google Scholar 

    93.
    Dezfuli, B. S., Maynard, B. J. & Wellnitz, T. A. Activity levels and predator detection by amphipods infected with an acanthocephalan parasite, Pomphorhynchus laevis. Folia Parasitol. (Praha) 50, 129–134 (2003).
    Google Scholar 

    94.
    Stone, C. F. & Moore, J. Parasite-induced alteration of odour responses in an amphipod-acanthocephalan system. Int. J. Parasitol. 44, 969–975 (2014).
    CAS  PubMed  Google Scholar 

    95.
    Jacquin, L., Mori, Q., Pause, M., Steffen, M. & Medoc, V. Non-specific manipulation of gammarid behaviour by P. minutus parasite enhances their predation by definitive bird hosts. PLoS ONE 9, e101684 (2014).
    ADS  PubMed  PubMed Central  Google Scholar 

    96.
    Thünken, T. et al. Impact of olfactory non-host predator cues on aggregation behaviour and activity in Polymorphus minutus infected Gammarus pulex. Hydrobiologia 654, 137–145 (2010).
    Google Scholar 

    97.
    Dianne, L. et al. Intraspecific conflict over host manipulation between different larval stages of an acanthocephalan parasite. J. Evol. Biol. 23, 2648–2655 (2010).
    CAS  PubMed  Google Scholar 

    98.
    Thomas, F., Brown, S. P., Sukhdeo, M. V. K. & Renaud, F. Understanding parasite strategies: A state-dependent approach?. Trends Parasitol. 18, 387–390 (2002).
    PubMed  Google Scholar 

    99.
    Baldauf, S. A. et al. Infection with an acanthocephalan manipulates an amphipod’s reaction to a fish predator’s odours. Int. J. Parasitol. 37, 61–65 (2007).
    PubMed  Google Scholar 

    100.
    Durieux, R., Rigaud, T. & Médoc, V. Parasite-induced suppression of aggregation under predation risk in a freshwater amphipod. Sociality of infected amphipods. Behav. Process. 91, 207–213 (2012).
    Google Scholar 

    101.
    Lewis, S. E., Hodel, A., Sturdy, T., Todd, R. & Weigl, C. Impact of acanthocephalan parasites on aggregation behavior of amphipods (Gammarus pseudolimnaeus). Behav. Process. 91, 159–163 (2012).
    Google Scholar 

    102.
    Labaude, S., Rigaud, T. & Cézilly, F. Host manipulation in the face of environmental changes: Ecological consequences. Int. J. Parasitol. Parasit. Wildl. 4, 442–451 (2015).
    Google Scholar 

    103.
    Rahmstorf, S. & Coumou, D. Increase of extreme events in a warming world. PNAS 108, 17905–17910 (2011).
    ADS  CAS  PubMed  Google Scholar  More

  • in

    Antarctica’s wilderness fails to capture continent’s biodiversity

    1.
    Mittermeier, R. A. et al. Wilderness and biodiversity conservation. Proc. Natl. Acad. Sci. USA 100, 10309–10313 (2003).
    ADS  CAS  PubMed  Google Scholar 
    2.
    Watson, J. E. M. et al. Protect the last of the wild. Nature 563, 27–30 (2018).
    ADS  CAS  PubMed  Google Scholar 

    3.
    Chown, S. L. et al. The changing form of Antarctic biodiversity. Nature 522, 431–438 (2015).
    ADS  CAS  PubMed  Google Scholar 

    4.
    Rintoul, S. R. et al. Choosing the future of Antarctica. Nature 558, 233–241 (2018).
    ADS  CAS  PubMed  Google Scholar 

    5.
    Pertierra, L. R., Hughes, K. A., Vega, G. C. & Olalla-Tárraga, M. Á. High resolution spatial mapping of human footprint across Antarctica and its implications for the strategic conservation of avifauna. PLoS One 12, e0168280 (2017).
    PubMed  PubMed Central  Google Scholar 

    6.
    Hughes, K. A., Fretwell, P., Rae, J., Holmes, K. & Fleming, A. Untouched Antarctica: mapping a finite and diminishing environmental resource. Antarct. Sci. 23, 537–548 (2011).
    ADS  Google Scholar 

    7.
    Secretariat of the Antarctic Treaty. Protocol on Environmental Protection to the Antarctic Treaty https://www.ats.aq/e/protocol.html (Antarctic Treaty Secretariat, 1991).

    8.
    Coetzee, B. W. T., Convey, P. & Chown, S. L. Expanding the protected area network in Antarctica is urgent and readily achievable. Conserv. Lett. 10, 670–680 (2017).
    Google Scholar 

    9.
    Keys, H. Towards Additional Protection of Antarctic Wilderness Areas https://documents.ats.aq/ATCM23/ip/ATCM23_ip080_e.doc (submitted by the Government of New Zealand, Doc. IP80, ATCM XXIII, 1999).

    10.
    Summerson, R. & Tin, T. Twenty years of protection of wilderness values in Antarctica. Polar J. 8, 265–288 (2018).
    Google Scholar 

    11.
    Di Marco, M., Ferrier, S., Harwood, T. D., Hoskins, A. J. & Watson, J. E. M. Wilderness areas halve the extinction risk of terrestrial biodiversity. Nature 573, 582–585 (2019).
    ADS  PubMed  Google Scholar 

    12.
    Cole, D. N. & Landres, P. B. Threats to wilderness ecosystems: impacts and research needs. Ecol. Appl. 6, 168–184 (1996).
    Google Scholar 

    13.
    Watson, J. E. M. et al. Catastrophic declines in wilderness areas undermine global environment targets. Curr. Biol. 26, 2929–2934 (2016).
    CAS  PubMed  Google Scholar 

    14.
    Lim, E. et al. Australian hot and dry extremes induced by weakenings of the stratospheric polar vortex. Nat. Geosci. 12, 896–901 (2019).
    ADS  CAS  Google Scholar 

    15.
    Summerson, R. & Riddle, M. J. in Antarctic Ecosystems: Models for Wider Ecological Understanding (eds Davison, W. et al.) 303–307 (New Zealand Natural Sciences, Christchurch, 2000).

    16.
    Bastmeijer, K. & van Hengel, S. The role of the protected area concept in protecting the world’s largest natural reserve: Antarctica. Utrecht Law Rev. 5, 61–79 (2009).
    Google Scholar 

    17.
    Chown, S. L. et al. Antarctica and the strategic plan for biodiversity. PLoS Biol. 15, e2001656 (2017).
    PubMed  PubMed Central  Google Scholar 

    18.
    Brooks, S. T., Jabour, J., van den Hoff, J. & Bergstrom, D. M. Our footprint on Antarctica competes with nature for rare ice-free land. Nat. Sustain. 2, 185–190 (2019).
    Google Scholar 

    19.
    Hughes, K. A. et al. Human-mediated dispersal of terrestrial species between Antarctic biogeographic regions: a preliminary risk assessment. J. Environ. Manage. 232, 73–89 (2019).
    PubMed  Google Scholar 

    20.
    Lee, J. R. et al. Climate change drives expansion of Antarctic ice-free habitat. Nature 547, 49–54 (2017).
    ADS  CAS  PubMed  Google Scholar 

    21.
    Hughes, K. A., Cowan, D. A. & Wilmotte, A. Protection of Antarctic microbial communities—‘out of sight, out of mind’. Front. Microbiol. 6, 151 (2015).
    PubMed  PubMed Central  Google Scholar 

    22.
    Hughes, K. A. et al. Pristine Antarctica: threats and protection. Antarct. Sci. 25, 1 (2013).
    ADS  Google Scholar 

    23.
    Shaw, J. D., Terauds, A., Riddle, M. J., Possingham, H. P. & Chown, S. L. Antarctica’s protected areas are inadequate, unrepresentative, and at risk. PLoS Biol. 12, e1001888 (2014).
    PubMed  PubMed Central  Google Scholar 

    24.
    Secretariat of the Antarctic Treaty. Antarctic Protected Areas Database https://www.ats.aq/devph/en/apa-database (2019).

    25.
    Committee for Environmental Protection (CEP). Understanding Concepts of Footprint and Wilderness Related to Protection of the Antarctic Environment https://documents.ats.aq/ATCM34/wp/ATCM34_wp035_e.doc (submitted by the Government of New Zealand, Doc. WP35, ATCM XXXIV, 2011).

    26.
    Committee for Environmental Protection (CEP). Annex V Inviolate and Reference Areas: Current Management Practices https://documents.ats.aq/ATCM35/ip/ATCM35_ip049_e.doc (submitted by ASOC, IP 49, ATCM XXXV, 2012).

    27.
    Committee for Environmental Protection (CEP). Report of the Twenty-second Meeting of the Committee for Environmental Protection https://documents.ats.aq/ATCM42/fr/ATCM42_fr001_e.pdf (CEP, 2019).

    28.
    Terauds, A. & Lee, J. R. Antarctic biogeography revisited: updating the Antarctic Conservation Biogeographic Regions. Divers. Distrib. 22, 836–840 (2016).
    Google Scholar 

    29.
    Council of Managers of National Antarctic Programs. Antarctic Facilities Operated by National Antarctic Programs in the Antarctic Treaty Area (South of 60° Latitude South) version 3.0.1 https://www.comnap.aq (COMNAP, accessed 8 August 2018).

    30.
    Tin, T., Liggett, D., Maher, P. T. & Lamers, M. (eds) Antarctic Futures: Human Engagement with the Antarctic Environment (Springer, Dordrecht, 2014).

    31.
    Dingwall, P. R. (ed.) Antarctica in the Environmental Era (Department of Conservation, Wellington, 1998).

    32.
    Summerson, R. in Protection of the Three Poles (ed. Huettmann, F.) 77–109 (Springer, Tokyo, 2012).

    33.
    Brooks, S. T., Tejedo, P. & O’Neill, T. A. Insights on the environmental impacts associated with visible disturbance of ice-free ground in Antarctica. Antarct. Sci. 31, 304–314 (2019).
    ADS  Google Scholar 

    34.
    O’Neill, T. A., Balks, M. R. & López-Martínez, J. Visual recovery of desert pavement surfaces following impacts from vehicle and foot traffic in the Ross Sea region of Antarctica. Antarct. Sci. 25, 514–530 (2013).
    ADS  Google Scholar 

    35.
    Convey, P. The influence of environmental characteristics on life history attributes of Antarctic terrestrial biota. Biol. Rev. Camb. Philos. Soc. 71, 191–225 (1996).
    Google Scholar 

    36.
    Ayres, E. et al. Effects of human trampling on populations of soil fauna in the McMurdo Dry Valleys, Antarctica. Conserv. Biol. 22, 1544–1551 (2008).
    PubMed  Google Scholar 

    37.
    Convey, P., Hughes, K. A. & Tin, T. Continental governance and environmental management mechanisms under the Antarctic Treaty System: sufficient for the biodiversity challenges of this century? Biodiversity (Nepean) 13, 234–248 (2012).
    Google Scholar 

    38.
    Chown, S. L. & Brooks, C. M. The state and future of Antarctic environments in a global context. Annu. Rev. Environ. Res. 44, 1–30 (2019).
    Google Scholar 

    39.
    Brooks, C. M. et al. Science-based management in decline in the Southern Ocean. Science 354, 185–187 (2016).
    CAS  PubMed  Google Scholar 

    40.
    Secretariat of the Antarctic Treaty. Revised Guidelines for Environmental Impact Assessment in Antarctica https://documents.ats.aq/recatt/Att605_e.pdf (Antarctic Treaty Secretariat, Buenos Aires, 2016).

    41.
    Agence Nationale Recherche. East Antarctic International Ice Sheet Traverse (DS0101) https://anr.fr/Project-ANR-16-CE01-0011 (ANR, France, 2016).

    42.
    Harris, C. M. et al. Important Bird Areas in Antarctica 2015 (BirdLife International and Environmental Research & Assessment Ltd., Cambridge, 2015).

    43.
    Cowan, D. A. et al. Non-indigenous microorganisms in the Antarctic: assessing the risks. Trends Microbiol. 19, 540–548 (2011).
    CAS  PubMed  Google Scholar 

    44.
    Montross, S. et al. Debris-rich basal ice as a microbial habitat, Taylor Glacier, Antarctica. Geomicrobiol. J. 31, 76–81 (2014).
    Google Scholar 

    45.
    Archer, S. D. J. et al. Airborne microbial transport limitation to isolated Antarctic soil habitats. Nat. Microbiol. 4, 925–932 (2019).
    CAS  PubMed  Google Scholar 

    46.
    Fretwell, P. T., Convey, P., Fleming, A. H., Peat, H. J. & Hughes, K. A. Detecting and mapping vegetation distribution on the Antarctic Peninsula from remote sensing data. Polar Biol. 34, 273–281 (2011).
    Google Scholar 

    47.
    Schwaller, M. R., Lynch, H. J., Tarroux, A. & Prehn, B. A continent-wide search for Antarctic petrel breeding sites with satellite remote sensing. Remote Sens. Environ. 210, 444–451 (2018).
    ADS  Google Scholar 

    48.
    Duffy, G. A. et al. Barriers to globally invasive species are weakening across the Antarctic. Divers. Distrib. 23, 982–996 (2017).
    Google Scholar 

    49.
    Consultative Parties to the Antarctic Treaty. Santiago Declaration https://www.ats.aq/documents/ATCM39/ad/atcm39_ad003_e.pdf (Antarctic Treaty Secretariat, Buenos Aires, 2016).
    Google Scholar 

    50.
    Pebesma, E. J. & Bivand, R. S. Classes and methods for spatial data in R. R News 5, 9–13 (2005).
    Google Scholar 

    51.
    R Core Team. R: a language and environment for statistical computing (R Foundation for Statistical Computing, Vienna, 2017).

    52.
    Environmental Systems Research Institute (ESRI). ArcGIS Desktop, release 10.6 (Environmental Systems Research Institute, Redlands, CA, 2011).

    53.
    Scientific Committee on Antarctic Research (SCAR). Antarctic Digital Database version 7 https://www.add.scar.org/ (2018).

    54.
    Headland, R. K. Chronological List of Antarctic Expeditions and Related Historical Events (Cambridge Univ. Press, Cambridge, 1989).
    Google Scholar 

    55.
    Scientific Committee on Antarctic Research. Composite Gazetteer of Antarctica https://data.aad.gov.au/aadc/gaz/scar/ (GCMD Metadata, 1992, updated 2014).

    56.
    Evans, J. S. spatialEco. R package version 0.0.1-7 https://CRAN.R-project.org/package=spatialEco (2017).

    57.
    Hijmans, R. J. raster: geographic data analysis and modeling. R package version 2.6-7 https://CRAN.R-project.org/package=raster (2017).

    58.
    Hughes, K. A. How committed are we to monitoring human impacts in Antarctica? Environ. Res. Lett. 5, 041001 (2010).
    ADS  Google Scholar 

    59.
    Bivand, R., Keitt, T. & Rowlingson, B. rgdal: bindings for the ‘geospatial’ data abstraction library. R package version 1.3-4 https://CRAN.R-project.org/package=rgdal (2018).

    60.
    International Association of Antarctica Tour Operators (IAATO). 2017–2018 Tourism Statistics http://iaato.org/tourism-statistics (IAATO, accessed 29 October 2018).

    61.
    United States Antarctic Program (USAP). USAP Science Planning Summaries 2003–2016 https://www.usap.gov/sciencesupport/2179/ (USAP, 2019).

    62.
    Bargagli, R. Antarctic Ecosystems: Environmental Contamination, Climate Change, and Human Impact (Springer, Berlin, 2005).

    63.
    Hughes, K. A. & Convey, P. The protection of Antarctic terrestrial ecosystems from inter- and intra-continental transfer of non-indigenous species by human activities: a review of current systems and practices. Glob. Environ. Change 20, 96–112 (2010).
    Google Scholar 

    64.
    Campbell, I. B., Claridge, G. G. C. & Balks, M. R. Short-and long-term impacts of human disturbances on snow-free surfaces in Antarctica. Polar Rec. (Gr. Brit.) 34, 15–24 (1998).
    Google Scholar 

    65.
    Tejedo, P. et al. Soil trampling in an Antarctic Specially Protected Area: tools to assess levels of human impact. Antarct. Sci. 21, 229–236 (2009).
    ADS  Google Scholar 

    66.
    Chown, S. L. et al. Continent-wide risk assessment for the establishment of nonindigenous species in Antarctica. Proc. Natl. Acad. Sci. USA 109, 4938–4943 (2012).
    ADS  CAS  PubMed  Google Scholar 

    67.
    Duffy, G. A. & Lee, J. R. Ice-free area expansion compounds the non-native species threat to Antarctic terrestrial biodiversity. Biol. Conserv. 232, 253–257 (2019).
    Google Scholar 

    68.
    Antarctica New Zealand. McMurdo Dry Valleys ASMA Manual 4th edn (Christchurch, New Zealand, 2015).

    69.
    BirdLife International. Antarctic Important Bird Areas http://datazone.birdlife.org/home (BirdLife International, Cambridge, 2018).

    70.
    Terauds, A. Antarctic Terrestrial Biodiversity Database (Australian Antarctic Data Centre, 2019).

    71.
    Casanovas, P., Black, M., Fretwell, P. & Convey, P. Mapping lichen distribution on the Antarctic Peninsula using remote sensing, lichen spectra and photographic documentation by citizen scientists. Polar Res. 34, 25633 (2015).
    Google Scholar 

    72.
    Fretwell, P. T. et al. An emperor penguin population estimate: the first global, synoptic survey of a species from space. PLoS One 7, e33751 (2012).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    73.
    Wauchope, H. S., Shaw, J. D. & Terauds, A. A snapshot of biodiversity protection in Antarctica. Nat. Commun. 10, 946 (2019).
    ADS  PubMed  PubMed Central  Google Scholar 

    74.
    Lynch, H. J., Naveen, R. & Fagan, W. F. Censuses of penguin, blue-eyed shag Phalacrocorax atriceps and southern giant petrel Macronectes giganteus populations on the Antarctic Peninsula, 2001-2007. Mar. Ornithol. 36, 83–97 (2008).
    Google Scholar 

    75.
    Burton-Johnson, A., Black, M., Fretwell, P. & Kaluza-Gilbert, J. An automated methodology for differentiating rock from snow, clouds and sea in Antarctica from Landsat 8 imagery: a new rock outcrop map and area estimation for the entire Antarctic continent. Cryosphere 10, 1665–1677 (2016).
    ADS  Google Scholar  More

  • in

    Determination of the most effective design for the measurement of photosynthetic light-response curves for planted Larix olgensis trees

    1.
    Henley, W. J. Measurement and interpretation of photosynthetic light response curves in algae in the context of photoinhibition and diel changes. J. Phycol. 29, 729–739 (1993).
    Article  Google Scholar 
    2.
    Kosugi, Y., Shibata, S. & Kobashi, S. Parameterization of the CO2 and H2O gas exchange of several temperate deciduous broad-leaved trees at the leaf scale considering seasonal changes. Plant Cell Environ. 26, 285–301 (2003).
    Article  Google Scholar 

    3.
    Mission, L., Tu, K. P., Boniello, R. A. & Goldstein, A. H. Seasonality of photosynthetic parameters in a multi-specific and vertically complex forest ecosystem in the Sierra Nevada of California. Tree Physiol. 26, 729–741 (2006).
    Article  Google Scholar 

    4.
    Coble, A. P., Vanderwall, B., Mau, A. & Cavaleri, M. How vertical patterns in leaf traits shift seasonally and the implications for modeling canopy photosynthesis in a temperate deciduous forest. Tree Physiol. 36, 1077–1091 (2016).
    CAS  Article  Google Scholar 

    5.
    Wilson, K. B., Baldocchi, D. D. & Hanson, P. J. Leaf age affects the seasonal pattern of photosynthetic capacity and net ecosystem exchange of carbon in a deciduous forest. Plant Cell Environ. 24, 571–583 (2011).
    Article  Google Scholar 

    6.
    Jin, S., Zhou, X. & Fan, J. Modeling daily photosynthesis of nine major tree species in northeast China. Forest Ecol. Manag. 184, 125–140 (2003).
    Article  Google Scholar 

    7.
    Zhang, X. Q. & Xu, D. Y. Eco-physiological modelling of canopy photosynthesis and growth of a Chinese fir plantation. Forest Ecol. Manag. 173, 201–211 (2003).
    Article  Google Scholar 

    8.
    Marino, G., Aqil, M. & Shipley, B. The leaf economics spectrum and the prediction of photosynthetic light-response curves. Funct. Ecol. 24, 263–272 (2010).
    Article  Google Scholar 

    9.
    Lachapelle, P. P. & Shipley, B. Interspecific prediction of photosynthetic light response curves using specific leaf mass and leaf nitrogen content: Effects of differences in soil fertility and growth irradiance. Ann. Bot. 109, 1149–1157 (2012).
    CAS  Article  Google Scholar 

    10.
    Xu, J. Z., Yu, Y. M., Peng, S. Z., Yang, S. H. & Liao, L. X. A modified nonrectangular hyperbola equation for photosynthetic light-response curves of leaves with different nitrogen status. Photosynthetica 52, 117–123 (2014).
    CAS  Article  Google Scholar 

    11.
    Calama, R., Puértolas, J., Madrigal, G. & Pardos, M. Modeling the environmental response of leaf net photosynthesis in Pinus pinea L. natural regeneration. Ecol. Model. 251, 9–21 (2013).
    Article  Google Scholar 

    12.
    Mayoral, C., Calama, R., Sánchez-González, M. & Pardos, M. Modelling the influence of light, water and temperature on photosynthesis in young trees of mixed Mediterranean forests. New For. 46, 485–506 (2015).
    Article  Google Scholar 

    13.
    Liu, Q., Dong, L. H. & Li, F. R. Modeling net CO2, assimilation (AN) within the crown of young planted Larix olgensis trees. Can. J. For. Res. 48, 1085–1098 (2018).
    CAS  Article  Google Scholar 

    14.
    Cavaleri, M. A., Oberbauer, S. F., Clark, D. B., Clark, D. A. & Ryan, M. G. Height is more important than light in determining leaf morphology in a tropical forest. Ecology 91, 1730–1739 (2010).
    Article  Google Scholar 

    15.
    Han, Q. Height-related decreases in mesophyll conductance, leaf photosynthesis and compensating adjustments associated with leaf nitrogen concentrations in Pinus densiflora. Tree Physiol. 31, 976–984 (2011).
    CAS  Article  Google Scholar 

    16.
    Kosugi, Y., Takanashi, S., Yokoyama, N. & Kamakura, M. Vertical variation in leaf gas exchange parameters for a Southeast Asian tropical rainforest in Peninsular Malaysia. J. Plant Res. 125, 735–748 (2012).
    Article  Google Scholar 

    17.
    Liu, Q., Dong, L. H., Li, F. R. & Xie, L. F. Spatial heterogeneity of canopy photosynthesis for Larix olgensis. Chin. J. Appl. Ecol. 27, 2789–2796 (2016) (in Chinese).
    Google Scholar 

    18.
    Liu, Q. & Li, F. R. Spatial and seasonal variations of standardized photosynthetic parameters under different environmental conditions for young planted Larix olgensis Henry Trees. Forests 9, 522 (2018).
    Article  Google Scholar 

    19.
    Ye, Z. P. A new model for relationship between irradiance and the rate of photosynthesis in Oryza sativa. Photosynthetica 45, 637–640 (2007).
    CAS  Article  Google Scholar 

    20.
    Mengistu, T., Sterck, F. J., Fetene, M., Tadesse, W. & Bongers, F. Leaf gas exchange in the frankincense tree (Boswellia papyrifera) of African dry woodlands. Tree Physiol. 31, 740–750 (2011).
    Article  Google Scholar 

    21.
    Chen, Z. Y., Peng, Z. S., Yang, J., Chen, W. Y. & Ou-Yang, Z. M. A mathematical model for describing light-response curves in Nicotiana tabacum L. Photosynthetica 49, 467–471 (2011).
    Google Scholar 

    22.
    Benomar, L., Desrochers, A. & Larocque, G. R. Changes in specific leaf area and photosynthetic nitrogen-use efficiency associated with physiological acclimation of two hybrid poplar clones to intraclonal competition. Can. J. For. Res. 41, 1465–1476 (2011).
    CAS  Article  Google Scholar 

    23.
    Ye, Z. P., Suggett, D. J., Robakowski, P. & Kang, H. J. A mechanistic model for the photosynthesis–light response based on the photosynthetic electron transport of photosystem II in C3 and C4 species. New Phytol. 199, 110–120 (2013).
    CAS  Article  Google Scholar 

    24.
    Xu, C. L., Sun, X. M., Zhang, S. G. & Dong, J. Maternal and paternal effects on photosynthetic characteristics of several Larix kaempferi × L. olgensis Hybrids . For. Res. 24, 8–12 (2011) (in Chinese).
    Google Scholar 

    25.
    Casella, E. & Ceulemans, R. Spatial distribution of leaf morphological and physiological characteristics in relation to local radiation regime within the canopies of 3-year-old Populus clones in coppice culture. Tree Physiol. 22, 1277–1288 (2002).
    CAS  Article  Google Scholar 

    26.
    Wieser, G., Oberhuber, W., Walder, L., Spieler, D. & Gruber, A. Photosynthetic temperature adaptation of Pinus cembra within the timberline ecotone of the Central Austrian Alps. Ann. For. Sci. 67, 201 (2010).
    Article  Google Scholar 

    27.
    Wang, Z., Kang, S., Jensen, C. R. & Liu, F. L. Alternate partial root-zone irrigation reduces bundle-sheath cell leakage to CO2 and enhances photosynthetic capacity in maize leaves. J. Exp. Bot. 63, 1145–1153 (2012).
    CAS  Article  Google Scholar 

    28.
    Quan, X. K. & Wang, C. K. Responses and influencing factors of foliar photosynthetic characteristics of Larix gmelinii to changing environments. Chin. Sci. Bull. 61, 2273–2286 (2016) (in Chinese).
    Article  Google Scholar 

    29.
    Posada, J. M., Lechowicz, M. J. & Kitajima, K. Optimal photosynthetic use of light by tropical tree crowns achieved by adjustment of individual leaf angles and nitrogen content. Ann. Bot. 103, 795–805 (2009).
    CAS  Article  Google Scholar 

    30.
    Rosati, A., Metcalf, S. G. & Lampinen, B. D. A simple method to estimate photosynthetic radiation use efficiency of canopies. Ann. Bot. 93, 567–574 (2004).
    CAS  Article  Google Scholar 

    31.
    Kern, S. O., Hovenden, M. J. & Jordan, G. J. The impacts of leaf shape and arrangement on light interception and potential photosynthesis in southern beech (Nothofagus cunninghamii). Funct. Plant Bio. 31, 471–480 (2004).
    Article  Google Scholar 

    32.
    Montalbán, I. A., De-Diego, N. & Moncaleán, P. Testing novel cytokinins for improved in vitro adventitious shoots formation and subsequent ex vitro performance in Pinus radiata. Forestry 84, 363–373 (2011).
    Article  Google Scholar 

    33.
    Lewis, J. D., Mckane, R. B., Tingey, D. T. & Beedlow, P. Vertical gradients in photosynthetic light response within an old-growth Douglas-fir and western hemlock canopy. Tree Physiol. 20, 447–456 (2000).
    Article  Google Scholar 

    34.
    Calder, W. J., Horn, K. J. & Clair, S. B. S. Conifer expansion reduces the competitive ability and herbivore defense of aspen by modifying light environment and soil chemistry. Tree Physiol. 31, 582–591 (2011).
    CAS  Article  Google Scholar 

    35.
    Joesting, H. M., Mccarthy, B. C. & Brown, K. J. The photosynthetic response of American chestnut seedlings to differing light conditions. Can. J. For. Res. 37, 1714–1722 (2007).
    CAS  Article  Google Scholar 

    36.
    Xu, L. & Baldocchi, D. D. Seasonal trends in photosynthetic parameters and stomatal conductance of blue oak (Quercus douglasii) under prolonged summer drought and high temperature. Tree Physiol. 23, 865–877 (2003).
    Article  Google Scholar 

    37.
    Wang, Q., Iio, A., Tenhunen, J. & Kakubari, Y. Annual and seasonal variations in photosynthetic capacity of Fagus crenata along an elevation gradient in the Naeba Mountains, Japan. Tree Physiol. 28, 277–285 (2008).
    Article  Google Scholar 

    38.
    Luo, Y. et al. Canopy quantum yield in a mesocosm study. Agric. For. Meteorol. 100, 35–48 (2000).
    ADS  Article  Google Scholar 

    39.
    Gardiner, E. S. & Krauss, K. W. Photosynthetic light response of flooded cherrybark oak (Quercus pagoda) seedlings grown in two light regimes. Tree Physiol. 21, 1103–1111 (2001).
    CAS  Article  Google Scholar 

    40.
    Wickham, H., Francois, R., Henry, L., Müller, K. RStudio. dplyr: A grammar of data manipulation. R Package Version 0.8.3. (2019). More

  • in

    Bacterial chemolithoautotrophy via manganese oxidation

    1.
    Beijerinck, M. Oxydation des mangancarbonates durch Bakterien und Schimmelpilze. Folia Microbiol. (Delft) 2, 123–134 (1913).
    Google Scholar 
    2.
    Nealson, K. H., Tebo, B. M. & Rosson, R. A. Occurrence and mechanisms of microbial oxidation of manganese. Adv. Appl. Microbiol. 33, 279–318 (1988).
    CAS  Google Scholar 

    3.
    Tebo, B. M., Johnson, H. A., McCarthy, J. K. & Templeton, A. S. Geomicrobiology of manganese(II) oxidation. Trends Microbiol. 13, 421–428 (2005).
    CAS  Google Scholar 

    4.
    Hansel, C. & Learman, D. R. in Ehrlich’s Geomicrobiology (eds Ehrlich, H. L. et al.) 401–452 (CRC, 2015).

    5.
    Myers, C. R. & Nealson, K. H. Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science 240, 1319–1321 (1988).
    ADS  CAS  Google Scholar 

    6.
    Lovley, D. R. & Phillips, E. J. Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl. Environ. Microbiol. 54, 1472–1480 (1988).
    CAS  PubMed  PubMed Central  Google Scholar 

    7.
    Winogradsky, S. Über schwefelbakterien. Bot. Ztg 45, 489ff (1887).
    Google Scholar 

    8.
    Kelly, D. P. & Wood, A. P. in The Prokaryotes: Prokaryotic Communities and Ecophysiology (eds Rosenberg, E. et al.) 275–287 (Springer, 2013).

    9.
    Daims, H. et al. Complete nitrification by Nitrospira bacteria. Nature 528, 504–509 (2015).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    10.
    Könneke, M. et al. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437, 543–546 (2005).
    ADS  Google Scholar 

    11.
    Strous, M. et al. Missing lithotroph identified as new planctomycete. Nature 400, 446–449 (1999).
    ADS  CAS  Google Scholar 

    12.
    van Kessel, M. A. H. J. et al. Complete nitrification by a single microorganism. Nature 528, 555–559 (2015).
    ADS  PubMed  PubMed Central  Google Scholar 

    13.
    Watson, S. W. & Waterbury, J. B. Characteristics of two marine nitrite oxidizing bacteria, Nitrospina gracilis nov. gen. nov. sp. and Nitrococcus mobilis nov. gen. nov. sp. Arch. Mikrobiol. 77, 203–230 (1971).
    Google Scholar 

    14.
    Lovley, D. R., Holmes, D. E. & Nevin, K. P. in Advances in Microbial Physiology (ed Poole, R. K.) 219–286 (Elsevier, 2004).

    15.
    Henkel, J. V. et al. A bacterial isolate from the Black Sea oxidizes sulfide with manganese(IV) oxide. Proc. Natl Acad. Sci. USA 116, 12153–12155 (2019).
    CAS  Google Scholar 

    16.
    Ghiorse, W. C. & Ehrlich, H. L. Microbial biomineralization of iron and manganese. Catena Suppl. 21, 75–99 (1992).
    Google Scholar 

    17.
    Ehrlich, H. L. & Salerno, J. C. Energy coupling in Mn2+ oxidation by a marine bacterium. Arch. Microbiol. 154, 12–17 (1990).
    CAS  Google Scholar 

    18.
    Ehrlich, H. L. Manganese as an energy source for bacteria. Environ. Biogeochem. 2, 633–644 (1976).
    CAS  Google Scholar 

    19.
    Dick, G. J. et al. Genomic insights into Mn(II) oxidation by the marine alphaproteobacterium Aurantimonas sp. strain SI85-9A1. Appl. Environ. Microbiol. 74, 2646–2658 (2008).
    CAS  PubMed  PubMed Central  Google Scholar 

    20.
    Nealson, K. H. in The Prokaryotes (eds Dworkin, M. et al.) 222–231 (Springer, 2006).

    21.
    van Veen, W. L. Biological oxidation of manganese in soils. Antonie van Leeuwenhoek 39, 657–662 (1973).
    Google Scholar 

    22.
    Morgan, J. J. Kinetics of reaction between O2 and Mn(II) species in aqueous solutions. Geochim. Cosmochim. Acta 69, 35–48 (2005).
    ADS  CAS  Google Scholar 

    23.
    Kits, K. D. et al. Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle. Nature 549, 269–272 (2017).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    24.
    Flagan, S. F. & Leadbetter, J. R. Utilization of capsaicin and vanillylamine as growth substrates by Capsicum (hot pepper)-associated bacteria. Environ. Microbiol. 8, 560–565 (2006).
    CAS  PubMed  PubMed Central  Google Scholar 

    25.
    Kanzler, B. E. M., Pfannes, K. R., Vogl, K. & Overmann, J. Molecular characterization of the nonphotosynthetic partner bacterium in the consortium “Chlorochromatium aggregatum”. Appl. Environ. Microbiol. 71, 7434–7441 (2005).
    CAS  PubMed  PubMed Central  Google Scholar 

    26.
    Emerson, D. & Moyer, C. Isolation and characterization of novel iron-oxidizing bacteria that grow at circumneutral pH. Appl. Environ. Microbiol. 63, 4784–4792 (1997).
    CAS  PubMed  PubMed Central  Google Scholar 

    27.
    Neidhardt, F. C. Escherichia coli and Salmonella: Cellular and Molecular Biology, vol. 1 (ASM, 1996).

    28.
    Kostanjšek, R., Pašić, L., Daims, H. & Sket, B. Structure and community composition of sprout-like bacterial aggregates in a dinaric karst subterranean stream. Microb. Ecol. 66, 5–18 (2013).
    Google Scholar 

    29.
    Wrighton, K. C. et al. Fermentation, hydrogen, and sulfur metabolism in multiple uncultivated bacterial phyla. Science 337, 1661–1665 (2012).
    ADS  CAS  Google Scholar 

    30.
    Parks, D. H. et al. Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nat. Microbiol. 2, 1533–1542 (2017).
    CAS  Google Scholar 

    31.
    Castelle, C. et al. A new iron-oxidizing/O2-reducing supercomplex spanning both inner and outer membranes, isolated from the extreme acidophile Acidithiobacillus ferrooxidans. J. Biol. Chem. 283, 25803–25811 (2008).
    CAS  PubMed  PubMed Central  Google Scholar 

    32.
    Jeans, C. et al. Cytochrome 572 is a conspicuous membrane protein with iron oxidation activity purified directly from a natural acidophilic microbial community. ISME J. 2, 542–550 (2008).
    CAS  Google Scholar 

    33.
    Croal, L. R., Jiao, Y. & Newman, D. K. The fox operon from Rhodobacter strain SW2 promotes phototrophic Fe(II) oxidation in Rhodobacter capsulatus SB1003. J. Bacteriol. 189, 1774–1782 (2007).
    CAS  Google Scholar 

    34.
    Jiao, Y. & Newman, D. K. The pio operon is essential for phototrophic Fe(II) oxidation in Rhodopseudomonas palustris TIE-1. J. Bacteriol. 189, 1765–1773 (2007).
    CAS  Google Scholar 

    35.
    He, S., Barco, R. A., Emerson, D. & Roden, E. E. Comparative genomic analysis of neutrophilic iron(II) oxidizer genomes for candidate genes in extracellular electron transfer. Front. Microbiol. 8, 1584 (2017).
    PubMed  PubMed Central  Google Scholar 

    36.
    Richardson, D. J. et al. The ‘porin-cytochrome’ model for microbe-to-mineral electron transfer. Mol. Microbiol. 85, 201–212 (2012).
    CAS  Google Scholar 

    37.
    Luther, G. W., III. Manganese(II) oxidation and Mn(IV) reduction in the environment—two one-electron transfer steps versus a single two-electron Step. Geomicrobiol. J. 22, 195–203 (2005).
    CAS  Google Scholar 

    38.
    Lücker, S. et al. A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria. Proc. Natl Acad. Sci. USA 107, 13479–13484 (2010).
    ADS  Google Scholar 

    39.
    Mundinger, A. B., Lawson, C. E., Jetten, M. S. M., Koch, H. & Lücker, S. Cultivation and transcriptional analysis of a canonical Nitrospira under stable growth conditions. Front. Microbiol. 10, 1325 (2019).
    PubMed  PubMed Central  Google Scholar 

    40.
    Koch, H. et al. Growth of nitrite-oxidizing bacteria by aerobic hydrogen oxidation. Science 345, 1052–1054 (2014).
    ADS  CAS  Google Scholar 

    41.
    Levicán, G., Ugalde, J. A., Ehrenfeld, N., Maass, A. & Parada, P. Comparative genomic analysis of carbon and nitrogen assimilation mechanisms in three indigenous bioleaching bacteria: predictions and validations. BMC Genomics 9, 581 (2008).
    PubMed  PubMed Central  Google Scholar 

    42.
    Berg, I. A. Ecological aspects of the distribution of different autotrophic CO2 fixation pathways. Appl. Environ. Microbiol. 77, 1925–1936 (2011).
    CAS  PubMed  PubMed Central  Google Scholar 

    43.
    Thauer, R. K., Jungermann, K. & Decker, K. Energy conservation in chemotrophic anaerobic bacteria. Bacteriol. Rev. 41, 100–180 (1977).
    CAS  PubMed  PubMed Central  Google Scholar 

    44.
    Baradaran, R., Berrisford, J. M., Minhas, G. S. & Sazanov, L. A. Crystal structure of the entire respiratory complex I. Nature 494, 443–448 (2013).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    45.
    Chadwick, G. L., Hemp, J., Fischer, W. W. & Orphan, V. J. Convergent evolution of unusual complex I homologs with increased proton pumping capacity: energetic and ecological implications. ISME J. 12, 2668–2680 (2018).
    CAS  PubMed  PubMed Central  Google Scholar 

    46.
    Lücker, S., Nowka, B., Rattei, T., Spieck, E. & Daims, H. The genome of Nitrospina gracilis illuminates the metabolism and evolution of the major marine nitrite oxidizer. Front. Microbiol. 4, 27 (2013).
    PubMed  PubMed Central  Google Scholar 

    47.
    Watson, S. W., Bock, E., Valois, F. W., Waterbury, J. B. & Schlosser, U. Nitrospira marina gen. nov. sp. nov.: a chemolithotrophic nitrite-oxidizing bacterium. Arch. Microbiol. 144, 1–7 (1986).
    Google Scholar 

    48.
    Hippe, H. Leptospirillum gen. nov. (ex Markosyan 1972), nom. rev., including Leptospirillum ferrooxidans sp. nov. (ex Markosyan 1972), nom. rev. and Leptospirillum thermoferrooxidans sp. nov. (Golovacheva et al. 1992). Int. J. Syst. Evol. Microbiol. 50, 501–503 (2000).
    Google Scholar 

    49.
    Henry, E. A. et al. Characterization of a new thermophilic sulfate-reducing bacterium Thermodesulfovibrio yellowstonii, gen. nov. and sp. nov.: its phylogenetic relationship to Thermodesulfobacterium commune and their origins deep within the bacterial domain. Arch. Microbiol. 161, 62–69 (1994).
    CAS  Google Scholar 

    50.
    Lin, X., Kennedy, D., Fredrickson, J., Bjornstad, B. & Konopka, A. Vertical stratification of subsurface microbial community composition across geological formations at the Hanford site. Environ. Microbiol. 14, 414–425 (2012).
    CAS  Google Scholar 

    51.
    Flagan, S., Ching, W.-K. & Leadbetter, J. R. Arthrobacter strain VAI-A utilizes acyl-homoserine lactone inactivation products and stimulates quorum signal biodegradation by Variovorax paradoxus. Appl. Environ. Microbiol. 69, 909–916 (2003).
    CAS  PubMed  PubMed Central  Google Scholar 

    52.
    Leadbetter, J. R. & Greenberg, E. P. Metabolism of acyl-homoserine lactone quorum-sensing signals by Variovorax paradoxus. J. Bacteriol. 182, 6921–6926 (2000).
    CAS  PubMed  PubMed Central  Google Scholar 

    53.
    Krumbein, W. E. & Altmann, H. J. A new method for the detection and enumeration of manganese oxidizing and reducing microorganisms. Helgol. Wiss. Meeresunters. 25, 347–356 (1973).
    CAS  Google Scholar 

    54.
    Emerson, D. & Revsbech, N. P. Investigation of an iron-oxidizing microbial mat community located near Aarhus, Denmark: laboratory studies. Appl. Environ. Microbiol. 60, 4032–4038 (1994).
    CAS  PubMed  PubMed Central  Google Scholar 

    55.
    Parada, A. E., Needham, D. M. & Fuhrman, J. A. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ. Microbiol. 18, 1403–1414 (2016).
    CAS  Google Scholar 

    56.
    Illumina. 16S Metagenomic sequencing library preparation, https://support.illumina.com/downloads/16s_metagenomic_sequencing_library_preparation.html (2013).

    57.
    Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336 (2010).
    CAS  PubMed  PubMed Central  Google Scholar 

    58.
    Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).
    CAS  Google Scholar 

    59.
    Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2013).
    CAS  Google Scholar 

    60.
    Lane, D. J. in Nucleic Acid Techniques in Bacterial Systematics (eds Stackebrandt, E. & Goodfellow, M.) 115–175 (John Wiley & Sons, 1991).

    61.
    Ludwig, W. et al. ARB: a software environment for sequence data. Nucleic Acids Res. 32, 1363–1371 (2004).
    CAS  PubMed  PubMed Central  Google Scholar 

    62.
    Parks, D. H. et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat. Biotechnol. 36, 996–1004 (2018).
    CAS  Google Scholar 

    63.
    Schönmann, S. et al. 16S rRNA gene-based phylogenetic microarray for simultaneous identification of members of the genus Burkholderia. Environ. Microbiol. 11, 779–800 (2009).
    Google Scholar 

    64.
    Greuter, D., Loy, A., Horn, M. & Rattei, T. probeBase—an online resource for rRNA-targeted oligonucleotide probes and primers: new features 2016. Nucleic Acids Res. 44, D586–D589 (2016).
    CAS  Google Scholar 

    65.
    Amann, R. I. et al. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl. Environ. Microbiol. 56, 1919–1925 (1990).
    CAS  PubMed  PubMed Central  Google Scholar 

    66.
    Stoecker, K., Dorninger, C., Daims, H. & Wagner, M. Double labeling of oligonucleotide probes for fluorescence in situ hybridization (DOPE-FISH) improves signal intensity and increases rRNA accessibility. Appl. Environ. Microbiol. 76, 922–926 (2010).
    CAS  PubMed  PubMed Central  Google Scholar 

    67.
    Schramm, A., Fuchs, B. M., Nielsen, J. L., Tonolla, M. & Stahl, D. A. Fluorescence in situ hybridization of 16S rRNA gene clones (Clone-FISH) for probe validation and screening of clone libraries. Environ. Microbiol. 4, 713–720 (2002).
    CAS  PubMed  PubMed Central  Google Scholar 

    68.
    Daims, H., Stoecker, K. & Wagner, M. in Molecular Microbial Ecology (eds Osborn, M. A. and Smith, C. J.) 208–228 (Taylor & Francis, 2004).

    69.
    Daims, H., Lücker, S. & Wagner, M. daime, a novel image analysis program for microbial ecology and biofilm research. Environ. Microbiol. 8, 200–213 (2006).
    CAS  Google Scholar 

    70.
    Taylor, G. J. & Crowder, A. A. Use of the DCB technique for extraction of hydrous iron oxides from roots of wetland plants. Am. J. Bot. 70, 1254 (1983).
    CAS  Google Scholar 

    71.
    Polerecky, L. et al. Look@NanoSIMS—a tool for the analysis of nanoSIMS data in environmental microbiology. Environ. Microbiol. 14, 1009–1023 (2012).
    CAS  Google Scholar 

    72.
    Brewer, P. G. & Spencer, D. W. Colorimetric determination of manganse in anoxic waters. Limnol. Oceanogr. 16, 107–110 (1971).
    ADS  CAS  Google Scholar 

    73.
    Oldham, V. E., Miller, M. T., Jensen, L. T. & Luther, G. W. Revisiting Mn and Fe removal in humic rich estuaries. Geochim. Cosmochim. Acta 209, 267–283 (2017).
    ADS  CAS  Google Scholar 

    74.
    Suzuki, M. T., Taylor, L. T. & DeLong, E. F. Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5′-nuclease assays. Appl. Environ. Microbiol. 66, 4605–4614 (2000).
    CAS  PubMed  PubMed Central  Google Scholar 

    75.
    William, S., Feil, H. & Copeland, A. Bacterial genomic DNA isolation using CTAB, Department of Energy Joint Genome Institute, https://jgi.doe.gov/user-programs/pmo-overview/protocols-sample-preparation-information/ (2012).

    76.
    Arkin, A. P. et al. KBase: the United States Department of Energy systems biology knowledgebase. Nat. Biotechnol. 36, 566–569 (2018).
    CAS  PubMed  PubMed Central  Google Scholar 

    77.
    Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
    CAS  PubMed  PubMed Central  Google Scholar 

    78.
    Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2012).
    MathSciNet  CAS  PubMed  PubMed Central  Google Scholar 

    79.
    Karst, S. M., Kirkegaard, R. H. & Albertsen, M. mmgenome: a toolbox for reproducible genome extraction from metagenomes. Preprint at https://www.biorxiv.org/content/ 10.1101/059121v1.full (2016).

    80.
    Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
    CAS  PubMed  PubMed Central  Google Scholar 

    81.
    Chen, I. A. et al. IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes. Nucleic Acids Res. 47, D666–D677 (2019).
    CAS  Google Scholar 

    82.
    NCBI Resource Coordinators. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 46, D8–D13 (2018).
    Google Scholar 

    83.
    Bagos, P. G., Liakopoulos, T. D., Spyropoulos, I. C. & Hamodrakas, S. J. PRED-TMBB: a web server for predicting the topology of β-barrel outer membrane proteins. Nucleic Acids Res. 32, W400–W404 (2004).
    CAS  PubMed  PubMed Central  Google Scholar 

    84.
    Federhen, S. The NCBI taxonomy database. Nucleic Acids Res. 40, D136–D143 (2012).
    CAS  Google Scholar 

    85.
    Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P. & Tyson, G. W. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043–1055 (2015).
    CAS  PubMed  PubMed Central  Google Scholar 

    86.
    Pruesse, E., Peplies, J. & Glöckner, F. O. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28, 1823–1829 (2012).
    CAS  PubMed  PubMed Central  Google Scholar 

    87.
    Ronquist, F. et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012).
    PubMed  PubMed Central  Google Scholar 

    88.
    Letunic, I. & Bork, P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 44, W242–W245 (2016).
    CAS  PubMed  PubMed Central  Google Scholar 

    89.
    Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).
    CAS  PubMed  PubMed Central  Google Scholar 

    90.
    Sievers, F. et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539 (2011).
    PubMed  PubMed Central  Google Scholar 

    91.
    Lever, M. A. et al. A modular method for the extraction of DNA and RNA, and the separation of DNA pools from diverse environmental sample types. Front. Microbiol. 6, 476 (2015).
    PubMed  PubMed Central  Google Scholar 

    92.
    Kopylova, E., Noé, L. & Touzet, H. SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics 28, 3211–3217 (2012).
    CAS  Google Scholar 

    93.
    Bray, N. L., Pimentel, H., Melsted, P. & Pachter, L. Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol. 34, 525–527 (2016).
    CAS  PubMed  Google Scholar 

    94.
    Pimentel, H., Bray, N. L., Puente, S., Melsted, P. & Pachter, L. Differential analysis of RNA-seq incorporating quantification uncertainty. Nat. Methods 14, 687–690 (2017).
    CAS  Google Scholar 

    95.
    van Waasbergen, L. G., Hildebrand, M. & Tebo, B. M. Identification and characterization of a gene cluster involved in manganese oxidation by spores of the marine Bacillus sp. strain SG-1. J. Bacteriol. 178, 3517–3530 (1996).
    PubMed  PubMed Central  Google Scholar 

    96.
    Jung, W. K. & Schweisfurth, R. Manganese oxidation by an intracellular protein of a Pseudomonas species. Z. Allg. Mikrobiol. 19, 107–115 (1979).
    CAS  Google Scholar 

    97.
    Esteve-Núñez, A., Rothermich, M., Sharma, M. & Lovley, D. Growth of Geobacter sulfurreducens under nutrient-limiting conditions in continuous culture. Environ. Microbiol. 7, 641–648 (2005).
    Google Scholar 

    98.
    Neubauer, S. C., Emerson, D. & Megonigal, J. P. Life at the energetic edge: kinetics of circumneutral iron oxidation by lithotrophic iron-oxidizing bacteria isolated from the wetland-plant rhizosphere. Appl. Environ. Microbiol. 68, 3988–3995 (2002).
    CAS  PubMed  PubMed Central  Google Scholar 

    99.
    Nowka, B., Daims, H. & Spieck, E. Comparison of oxidation kinetics of nitrite-oxidizing bacteria: nitrite availability as a key factor in niche differentiation. Appl. Environ. Microbiol. 81, 745–753 (2015).
    PubMed  PubMed Central  Google Scholar 

    100.
    Ehrich, S., Behrens, D., Lebedeva, E., Ludwig, W. & Bock, E. A new obligately chemolithoautotrophic, nitrite-oxidizing bacterium, Nitrospira moscoviensis sp. nov. and its phylogenetic relationship. Arch. Microbiol. 164, 16–23 (1995).
    CAS  Google Scholar 

    101.
    Kim, S. & Lee, S. B. Catalytic promiscuity in dihydroxy-acid dehydratase from the thermoacidophilic archaeon Sulfolobus solfataricus. J. Biochem. 139, 591–596 (2006).
    CAS  Google Scholar 

    102.
    Safarian, S. et al. Structure of a bd oxidase indicates similar mechanisms for membrane-integrated oxygen reductases. Science 352, 583–586 (2016).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    103.
    Lovley, D. R. & Phillips, E. J. P. Manganese inhibition of microbial iron reduction in anaerobic sediments. Geomicrobiol. J. 6, 145–155 (1988).
    CAS  Google Scholar 

    104.
    Perez-Benito, J. F., Arias, C. & Amat, E. A kinetic study of the reduction of colloidal manganese dioxide by oxalic acid. J. Colloid Interface Sci. 177, 288–297 (1996).
    ADS  CAS  Google Scholar  More

  • in

    Identifying hotspots of invasive alien terrestrial vertebrates in Europe to assist transboundary prevention and control

    1.
    Bellard, C., Cassey, P. & Blackburn, T. M. Alien species as a driver of recent extinctions. Biol. Lett. 12, 20150623 (2016).
    PubMed  PubMed Central  Google Scholar 
    2.
    IPBES. Global Assessment Report on Biodiversity and Ecosystem Services. (2019).

    3.
    Courchamp, F., Chapuis, J. L. & Pascal, M. Mammal invaders on islands: Impact, control and control impact. Biol. Rev. Camb. Philos. Soc. 78, 347–383 (2003).
    PubMed  Google Scholar 

    4.
    Simberloff, D. et al. Impacts of biological invasions: What’s what and the way forward. Trends Ecol. Evol. 28, 58–66 (2013).
    PubMed  Google Scholar 

    5.
    Pimentel, D., Lach, L., Zuniga, R. & Morrison, D. Environmental and economic costs of nonindigenous species in the United States. Bioscience 50, 53–65 (2000).
    Google Scholar 

    6.
    Kettunen, M. et al. Technical support to EU strategy on invasive species (IAS). Assessment of the impacts of IAS in Europe and the EU. (2009).

    7.
    Katsanevakis, S. European Alien Species Information Network (EASIN): Supporting European policies and scientific research. Manag. Biol. Invasions 6, 147–157 (2015).
    Google Scholar 

    8.
    Hulme, P. E., Pysek, P., Nentwig, W. & Vilà, M. Will threat of biological invasions unite the European Union ?. Science (80-). 324, 40–41 (2009).
    ADS  CAS  Google Scholar 

    9.
    UNEP. Convention on Biological Diversity. (1992).

    10.
    EU Council. Council Decision of 25 October 1993 concerning the conclusion of the Convention on Biological Diversity. 1–20 (1993).

    11.
    Carboneras, C. et al. A prioritised list of invasive alien species to assist the effective implementation of EU legislation. J. Appl. Ecol. 55, 539–547 (2018).
    Google Scholar 

    12.
    Stohlgren, T. J. & Schnase, J. L. Risk analysis for biological hazards: What we need to know about invasive species. Risk Anal. 26, 163–173 (2006).
    PubMed  Google Scholar 

    13.
    Soberón, J. M. Niche and area of distribution modeling: A population ecology perspective. Ecography (Cop.) 33, 159–167 (2010).
    Google Scholar 

    14.
    Guisan, A. & Thuiller, W. Predicting species distribution: Offering more than simple habitat models. Ecol. Lett. 8, 993–1009 (2005).
    Google Scholar 

    15.
    Gallien, L., Douzet, R., Pratte, S., Zimmermann, N. E. & Thuiller, W. Invasive species distribution models: How violating the equilibrium assumption can create new insights. Glob. Ecol. Biogeogr. 21, 1126–1136 (2012).
    Google Scholar 

    16.
    Jeschke, J. M. & Strayer, D. L. Usefulness of bioclimatic models for studying climate change and invasive species. Ann. N. Y. Acad. Sci. 1134, 1–24 (2008).
    ADS  PubMed  Google Scholar 

    17.
    Vilà, M. et al. How well do we understand the impacts of alien species on ecosystem services? A pan-European, cross-taxa assessment. Front. Ecol. Environ. 8, 135–144 (2010).
    Google Scholar 

    18.
    DAISIE. Handbook of Alien Species in Europe. Invading Nature: Springer Series in Invasion Ecology. Invading Nature. Springer Series in Invasion Ecology Vol. 3 (Springer, New York, 2009).
    Google Scholar 

    19.
    McCullogh, D. R., Takatsuki, S. & Kaji, K. Sika Deer. Biology and Management of Native and Introduced Populations (Springer, New York, 2009). https://doi.org/10.1017/CBO9781107415324.004.

    20.
    Reyns, N. et al. Cost-benefit analysis for invasive species control: The case of greater Canada goose Branta canadensis in Flanders (northern Belgium). PeerJ 6, e4283 (2018).
    PubMed  PubMed Central  Google Scholar 

    21.
    Vourc’h, G., Marmet, J., Chassagne, M., Bord, S. & Chapuis, J.-L. Borrelia burgdorferi Sensu Lato in Siberian Chipmunks (Tamias sibiricus) introduced in suburban forests in France. Vector-Borne Zoonotic Dis. 7, 637–642 (2007).
    PubMed  Google Scholar 

    22.
    Nentwig, W. Biological Invasions Vol. 193 (Springer Science & Business Media, New York, 2007).
    Google Scholar 

    23.
    Miaud, C. et al. Invasive North American bullfrogs transmit lethal fungus Batrachochytrium dendrobatidis infections to native amphibian host species. Biol. Invasions 18, 2299–2308 (2016).
    Google Scholar 

    24.
    GBIF.org. GBIF Home Page. (2019). https://www.gbif.org.

    25.
    Gallardo, B., Zieritz, A. & Aldridge, D. C. The importance of the human footprint in shaping the global distribution of terrestrial, freshwater and marine invaders. PLoS ONE 10, 1–17 (2015).
    Google Scholar 

    26.
    Dawson, W. et al. Global hotspots and correlates of alien species richness across taxonomic groups. Nat. Ecol. Evol. 1, 1–7 (2017).
    Google Scholar 

    27.
    Gallardo, B. et al. Protected areas offer refuge from invasive species spreading under climate change. Glob. Change Biol. 23, 5331–5343 (2017).
    ADS  Google Scholar 

    28.
    Pitt, W. C. & Witmer, G. W. Invasive vertebrate species and the challenges of management. In Proceedings of the Vertebrate Pest Conference, Vol. 1779 (2014).

    29.
    Genovesi, P. Eradications of invasive alien species in Europe: A review. Biol. Invasions 1995, 127–133 (2005).
    Google Scholar 

    30.
    Kark, S. et al. Cross-boundary collaboration: Key to the conservation puzzle. Curr. Opin. Environ. Sustain. 12, 12–24 (2015).
    Google Scholar 

    31.
    Wittenberg, R. & Cock, M. J. W. Invasive Alien Species: A Toolkit of Best Prevention and Management Practices (CAB International, Wallingford, 2001).
    Google Scholar 

    32.
    Yiming, L., Zhengjun, W. & Duncan, R. P. Why islands are easier to invade: Human influences on bullfrog invasion in the Zhoushan archipelago and neighboring mainland China. Oecologia 148, 129–136 (2006).
    ADS  PubMed  Google Scholar 

    33.
    Kaji, K., Miyaki, M., Saitoh, T., Ono, S. & Kaneko, M. Spatial distribution of an expanding sika deer population on Hokkaido Island, Japan. Wildl. Soc. Bull. 28, 699–707 (2000).
    Google Scholar 

    34.
    Nordstrom, M. et al. Effects of feral mink removal on seabirds, waders and passerines on small islands in the Baltic Sea. Biol. Conserv. 109, 359–368 (2003).
    Google Scholar 

    35.
    Bellard, C. et al. Will climate change promote future invasions?. Glob. Change Biol. 19, 3740–3748 (2013).
    ADS  Google Scholar 

    36.
    Hattab, T. et al. A unified framework to model the potential and realized distributions of invasive species within the invaded range. Divers. Distrib. 23, 806–819 (2017).
    Google Scholar 

    37.
    Roy, H. E. et al. Developing a list of invasive alien species likely to threaten biodiversity and ecosystems in the European Union. Glob. Change Biol. 25, 1032–1048 (2019).
    ADS  Google Scholar 

    38.
    Union, E. Regulation (EU) No 1143/2014 of the European Parliament and the Council of 22 October 2014 on the prevention and management of the introduction and spread of invasive alien species. Off. J. Eur. Union 317, 35–55 (2014).
    Google Scholar 

    39.
    Rodríguez-Sanchez, F., Pérez-Luque, A. J., Bartomeus, I. & Varela, S. Ciencia reproducible: ¿qué, por qué, cómo?. Ecosistemas 25, 83–92 (2016).
    Google Scholar 

    40.
    Katsanevakis, S. et al. Implementing the European policies for alien species—networking, science, and partnership in a complex environment. Manag. Biol. Invasions 4, 3–6 (2013).
    Google Scholar 

    41.
    Rocchini, D. et al. Accounting for uncertainty when mapping species distributions: The need for maps of ignorance. Prog. Phys. Geogr. 35, 211–226 (2011).
    Google Scholar 

    42.
    Jiménez-Valverde, A. et al. Use of niche models in invasive species risk assessments. Biol. Invasions 13, 2785–2797 (2011).
    Google Scholar 

    43.
    Brook, B. W., Sodhi, N. S. & Bradshaw, C. J. A. Synergies among extinction drivers under global change. Trends Ecol. Evol. 23, 453–460 (2008).
    PubMed  Google Scholar 

    44.
    Latham, A. D. M., Latham, M. C., Cieraad, E., Tompkins, D. M. & Warburton, B. Climate change turns up the heat on vertebrate pest control. Biol. Invasions 17, 2821–2829 (2015).
    Google Scholar 

    45.
    Hurtt, G. C. et al. Harmonization of land-use scenarios for the period 1500–2100: 600 years of global gridded annual land-use transitions, wood harvest, and resulting secondary lands. Clim. Change 109, 117–161 (2011).
    ADS  Google Scholar 

    46.
    Union, E. EU Regulation No 1143/2014 on the prevention and management of the introduction and spread of invasive alien species. Off. J. Eur. Union 317, 35–55 (2014).
    Google Scholar 

    47.
    Beaumont, L. J. et al. Different climatic envelopes among invasive populations may lead to underestimations of current and future biological invasions. Divers. Distrib. 15, 409–420 (2009).
    Google Scholar 

    48.
    R Core Team. R: A language and environment for statistical computing. (2019).

    49.
    Karger, D. N. et al. Climatologies at high resolution for the earth’s land surface areas. Sci. Data 4, 1–20 (2017).
    Google Scholar 

    50.
    Natural Earth. Rivers and lake centerlines. https://www.naturalearthdata.com/downloads/10m-physical-vectors/10m-rivers-lake-centerlines/. (2018).

    51.
    EEA. Corine Land Cover (CLC), Copernicus Land Monitoring Service. (2018).

    52.
    LP DAAC. Global 30 arc-second elevation data set GTOPO30. Land Process Distributed Active Archive Center (2004). https://edcdaac.usgs.gov/gtopo30/gtopo30.asp. Accessed 1st Sep 2017.

    53.
    Nelson, A. Estimated travel time to the nearest city of 50,000 or more people in year 2000. Global Environment Monitoring Unit-Joint Research Centre of the European Comission (2008). https://bioval.jrc.ec.europa.eu/products/gam/. Accessed 1st Oct 2017.

    54.
    Naimi, B. Package ‘ usdm ’: Uncertainty analysis for species distribution models. (2017).

    55.
    Chamberlain, S. et al. rgbif: Interface to the Global Biodiversity Information Facility API. R package version 1.3.0. https://cran.r-project.org/package=rgbif. (2019).

    56.
    Pysek, P. et al. Geographical and taxonomic biases in invasion ecology. Trends Ecol. Evol. 23, 237–244 (2008).
    PubMed  Google Scholar 

    57.
    Scharn, R. et al. CoordinateCleaner: Standardized cleaning of occurrence records from biological collection databases. Methods Ecol. Evol. 2019, 1–8 (2019).
    Google Scholar 

    58.
    Beck, J., Böller, M., Erhardt, A. & Schwanghart, W. Spatial bias in the GBIF database and its effect on modeling species’ geographic distributions. Ecol. Inform. 19, 10–15 (2014).
    Google Scholar 

    59.
    Thuiller, A. W., Georges, D., Engler, R., Georges, M. D. & Thuiller, C. W. The biomod2 package: The updated object-oriented version of BIOMOD package. Manag. Biol. Invasions https://doi.org/10.1098/Rspb.2014.1776 (2016).
    Article  Google Scholar 

    60.
    Araújo, M. B. & New, M. Ensemble forecasting of species distributions. Trends Ecol. Evol. 22, 42–47 (2007).
    PubMed  PubMed Central  Google Scholar 

    61.
    Hirzel, A. H., Randin, C. & Guisan, A. Evaluating the ability of habitat suitability models to predict species presences. Ecol. Model. 9, 142–152 (2006).
    Google Scholar 

    62.
    Allouche, O., Tsoar, A. & Kadmon, R. Assessing the accuracy of species distribution models: Prevalence, kappa and the true skill statistic (TSS). J. Appl. Ecol. 43, 1223–1232 (2006).
    Google Scholar 

    63.
    Liu, C., White, M. & Newell, G. Selecting thresholds for the prediction of species occurrence with presence-only data. J. Biogeogr. 40, 778–789 (2013).
    Google Scholar 

    64.
    Hijmans, R. J., Phillips, S., Leathwick, J. R. & Elith, J. Dismo package for R, version 1.1-4. Circles https://doi.org/10.1016/j.jhydrol.2011.07.022 (2017).
    Article  Google Scholar 

    65.
    Ruete, A. Displaying bias in sampling effort of data accessed from biodiversity databases using ignorance maps. Biodivers. Data J. 3, e5361 (2015).
    Google Scholar 

    66.
    QGIS Development Team. QGIS Geographic Information System. (2018).

    67.
    DAISIE. Handbook of Alien Species in Europe. Invading nature. Springer series in invasion ecology 3 (Springer, New York, 2009).
    Google Scholar 

    68.
    CABI. Invasive Species Compendium. (2020). More

  • in

    Bifidobacterial biofilm formation is a multifactorial adaptive phenomenon in response to bile exposure

    1.
    Flemming, H.-C. et al. Biofilms: an emergent form of bacterial life. Nat. Rev. Microbiol. 14, 563. https://doi.org/10.1038/nrmicro.2016.94 (2016).
    CAS  Article  PubMed  Google Scholar 
    2.
    Boddey, J. A., Flegg, C. P., Day, C. J., Beacham, I. R. & Peak, I. R. Temperature-regulated microcolony formation by Burkholderia pseudomallei requires pilA and enhances association with cultured human cells. Infect. Immunity 74, 5374–5381. https://doi.org/10.1128/iai.00569-06 (2006).
    CAS  Article  Google Scholar 

    3.
    Lister, J. L. & Horswill, A. R. Staphylococcus aureus biofilms: recent developments in biofilm dispersal. Front. Cell. Infect. Microbiol. https://doi.org/10.3389/fcimb.2014.00178 (2014).
    Article  PubMed  PubMed Central  Google Scholar 

    4.
    Whitchurch, C. B., Tolker-Nielsen, T., Ragas, P. C. & Mattick, J. S. Extracellular DNA required for bacterial biofilm formation. Science 295, 1487–1487. https://doi.org/10.1126/science.295.5559.1487 (2002).
    CAS  Article  PubMed  Google Scholar 

    5.
    Foster, T. J., Geoghegan, J. A., Ganesh, V. K. & Höök, M. Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Nat. Rev. Microbiol. 12, 49. https://doi.org/10.1038/nrmicro3161 (2013).
    CAS  Article  Google Scholar 

    6.
    Mack, D. et al. The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear beta-1,6-linked glucosaminoglycan: purification and structural analysis. J. Bacteriol. 178, 175–183 (1996).
    CAS  Article  Google Scholar 

    7.
    Limoli, D. H., Jones, C. J. & Wozniak, D. J. Bacterial extracellular polysaccharides in biofilm formation and function. Microbiol. Spectrum. https://doi.org/10.1128/microbiolspec.MB-0011-2014 (2015).
    Article  Google Scholar 

    8.
    Gallaher, T. K., Wu, S., Webster, P. & Aguilera, R. Identification of biofilm proteins in non-typeable Haemophilus Influenzae. BMC Microbiol. 6, 65. https://doi.org/10.1186/1471-2180-6-65 (2006).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    9.
    Hu, W. et al. DNA builds and strengthens the extracellular matrix in Myxococcus xanthus biofilms by interacting with exopolysaccharides. PLoS ONE 7, e51905. https://doi.org/10.1371/journal.pone.0051905 (2012).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    10.
    Boles, B. R. & Horswill, A. R. Staphylococcal biofilm disassembly. Trends Microbiol. 19, 449–455. https://doi.org/10.1016/j.tim.2011.06.004 (2011).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    11.
    Reen, F. J. et al. Bile signalling promotes chronic respiratory infections and antibiotic tolerance. Sci. Rep. 6, 29768 (2016).
    ADS  CAS  Article  Google Scholar 

    12.
    Duanis-Assaf, D., Steinberg, D., Chai, Y. & Shemesh, M. The LuxS based quorum sensing governs lactose induced biofilm formation by Bacillus subtilis. Front. Microbiol. https://doi.org/10.3389/fmicb.2015.01517 (2016).
    Article  PubMed  PubMed Central  Google Scholar 

    13.
    Le, K. Y. & Otto, M. Quorum-sensing regulation in staphylococci-an overview. Front. Microbiol. 6, 1174–1174. https://doi.org/10.3389/fmicb.2015.01174 (2015).
    Article  PubMed  PubMed Central  Google Scholar 

    14.
    Qi, L. et al. Relationship between antibiotic resistance, biofilm formation, and biofilm-specific resistance in Acinetobacter baumannii. Front. Microbiol. 7, 483–483. https://doi.org/10.3389/fmicb.2016.00483 (2016).
    Article  PubMed  PubMed Central  Google Scholar 

    15.
    O’Callaghan, A. & van Sinderen, D. Bifidobacteria and their role as members of the human gut microbiota. Front. Microbiol. 7, 925–925. https://doi.org/10.3389/fmicb.2016.00925 (2016).
    Article  PubMed  PubMed Central  Google Scholar 

    16.
    Hill, C. et al. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol. 11, 506. https://doi.org/10.1038/nrgastro.2014.66 (2014).
    Article  PubMed  Google Scholar 

    17.
    Sánchez, B., Ruiz, L., Gueimonde, M., Ruas-Madiedo, P. & Margolles, A. Adaptation of bifidobacteria to the gastrointestinal tract and functional consequences. Pharmacol. Res. 69, 127–136. https://doi.org/10.1016/j.phrs.2012.11.004 (2013).
    Article  PubMed  Google Scholar 

    18.
    Holm, R., Müllertz, A. & Mu, H. Bile salts and their importance for drug absorption. Int. J. Pharm. 453, 44–55. https://doi.org/10.1016/j.ijpharm.2013.04.003 (2013).
    CAS  Article  PubMed  Google Scholar 

    19.
    Islam, K. B. M. S. et al. Bile acid is a host factor that regulates the composition of the cecal microbiota in rats. Gastroenterology 141, 1773–1781. https://doi.org/10.1053/j.gastro.2011.07.046 (2011).
    CAS  Article  PubMed  Google Scholar 

    20.
    Begley, M., Gahan, C. G. & Hill, C. The interaction between bacteria and bile. FEMS Microbiol. Rev. 29, 625–651. https://doi.org/10.1016/j.femsre.2004.09.003 (2005).
    CAS  Article  PubMed  Google Scholar 

    21.
    Ruiz, L., Margolles, A. & Sanchez, B. Bile resistance mechanisms in Lactobacillus and Bifidobacterium. Front. Microbiol. 4, 396. https://doi.org/10.3389/fmicb.2013.00396 (2013).
    Article  PubMed  PubMed Central  Google Scholar 

    22.
    Price, C. E., Reid, S. J., Driessen, A. J. & Abratt, V. R. The Bifidobacterium longum NCIMB 702259T ctr gene codes for a novel cholate transporter. Appl. Environ. Microbiol. 72, 923–926. https://doi.org/10.1128/aem.72.1.923-926.2006 (2006).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    23.
    Gueimonde, M., Garrigues, C., van Sinderen, D., de los Reyes-Gavilan, C. G. & Margolles, A. Bile-inducible efflux transporter from Bifidobacterium longum NCC2705, conferring bile resistance. Appl. Environ. Microbiol. 75, 3153–3160. https://doi.org/10.1128/aem.00172-09 (2009).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    24.
    Ruiz, L., Zomer, A., O’Connell-Motherway, M., van Sinderen, D. & Margolles, A. Discovering novel bile protection systems in Bifidobacterium breve UCC2003 through functional genomics. Appl. Environ. Microbiol. 78, 1123–1131. https://doi.org/10.1128/aem.06060-11 (2012).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    25.
    Ruiz, L., Sánchez, B., Ruas-Madiedo, P., De Los Reyes-Gavilán, C. G. & Margolles, A. Cell envelope changes in Bifidobacterium animalis ssp. lactis as a response to bile. FEMS Microbiol. Lett. 274, 316–322. https://doi.org/10.1111/j.1574-6968.2007.00854.x (2007).
    CAS  Article  PubMed  Google Scholar 

    26.
    Gómez Zavaglia, A., Kociubinski, G., Pérez, P., Disalvo, E. & De Antoni, G. Effect of bile on the lipid composition and surface properties of bifidobacteria. J. Appl. Microbiol. 93, 794–799. https://doi.org/10.1046/j.1365-2672.2002.01747.x (2002).
    Article  PubMed  Google Scholar 

    27.
    An, H. et al. Integrated transcriptomic and proteomic analysis of the bile stress response in a centenarian-originated probiotic Bifidobacterium longum BBMN68. Mol. Cell. Proteom. 13, 2558–2572. https://doi.org/10.1074/mcp.M114.039156 (2014).
    CAS  Article  Google Scholar 

    28.
    Sanchez, B., de los Reyes-Gavilan, C. G. & Margolles, A. The F1F0-ATPase of Bifidobacterium animalis is involved in bile tolerance. Environ. Microbiol. 8, 1825–1833. https://doi.org/10.1111/j.1462-2920.2006.01067.x (2006).
    CAS  Article  PubMed  Google Scholar 

    29.
    Sanchez, B., Noriega, L., Ruas-Madiedo, P., de los Reyes-Gavilan, C. G. & Margolles, A. Acquired resistance to bile increases fructose-6-phosphate phosphoketolase activity in Bifidobacterium. FEMS Microbiol. Lett. 235, 35–41. https://doi.org/10.1016/j.femsle.2004.04.009 (2004).
    CAS  Article  PubMed  Google Scholar 

    30.
    Sanchez, B. et al. Proteomic analysis of global changes in protein expression during bile salt exposure of Bifidobacterium longum NCIMB 8809. J. Bacteriol. 187, 5799–5808. https://doi.org/10.1128/jb.187.16.5799-5808.2005 (2005).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    31.
    Noriega, L., Gueimonde, M., Sanchez, B., Margolles, A. & de los Reyes-Gavilan, C. G. Effect of the adaptation to high bile salts concentrations on glycosidic activity, survival at low PH and cross-resistance to bile salts in Bifidobacterium. Int. J. Food Microbiol. 94, 79–86. https://doi.org/10.1016/j.ijfoodmicro.2004.01.003 (2004).
    CAS  Article  PubMed  Google Scholar 

    32.
    Tanaka, H., Hashiba, H., Kok, J. & Mierau, I. Bile salt hydrolase of Bifidobacterium longum-biochemical and genetic characterization. Appl. Environ. Microbiol. 66, 2502–2512. https://doi.org/10.1128/aem.66.6.2502-2512.2000 (2000).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    33.
    Noriega, L., Cuevas, I., Margolles, A. & de los Reyes-Gavilán, C. G. Deconjugation and bile salts hydrolase activity by Bifidobacterium strains with acquired resistance to bile. Int. Dairy J. 16, 850–855. https://doi.org/10.1016/j.idairyj.2005.09.008 (2006).
    CAS  Article  Google Scholar 

    34.
    Ambalam, P., Kondepudi, K. K., Nilsson, I., Wadstrom, T. & Ljungh, A. Bile enhances cell surface hydrophobicity and biofilm formation of bifidobacteria. Appl. Biochem. Biotechnol. 172, 1970–1981. https://doi.org/10.1007/s12010-013-0596-1 (2014).
    CAS  Article  PubMed  Google Scholar 

    35.
    Pumbwe, L. et al. Bile salts enhance bacterial co-aggregation, bacterial-intestinal epithelial cell adhesion, biofilm formation and antimicrobial resistance of Bacteroides fragilis. Microb. Pathog. 43, 78–87. https://doi.org/10.1016/j.micpath.2007.04.002 (2007).
    CAS  Article  PubMed  Google Scholar 

    36.
    Lebeer, S., Verhoeven, T. L., Perea Velez, M., Vanderleyden, J. & De Keersmaecker, S. C. Impact of environmental and genetic factors on biofilm formation by the probiotic strain Lactobacillus rhamnosus GG. Appl. Environ. Microbiol. 73, 6768–6775. https://doi.org/10.1128/aem.01393-07 (2007).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    37.
    Macfarlane, S. & Macfarlane, G. T. Composition and metabolic activities of bacterial biofilms colonizing food residues in the human gut. Appl. Environ. Microbiol. 72, 6204–6211. https://doi.org/10.1128/aem.00754-06 (2006).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    38.
    Macfarlane, M. J. H. G. T. M. S. Bacterial growth and metabolism on surfaces in the large intestine. Microb. Ecol. Health Dis. 12, 64–72. https://doi.org/10.1080/089106000750060314 (2000).
    Article  Google Scholar 

    39.
    Pereira, C. S., Thompson, J. A. & Xavier, K. B. AI-2-mediated signalling in bacteria. FEMS Microbiol. Rev. 37, 156–181. https://doi.org/10.1111/j.1574-6976.2012.00345.x (2013).
    CAS  Article  PubMed  Google Scholar 

    40.
    Hammer, B. K. & Bassler, B. L. Quorum sensing controls biofilm formation in Vibrio cholerae. Mol. Microbiol. 50, 101–104. https://doi.org/10.1046/j.1365-2958.2003.03688.x (2003).
    CAS  Article  PubMed  Google Scholar 

    41.
    Solano, C., Echeverz, M. & Lasa, I. Biofilm dispersion and quorum sensing. Curr. Opin. Microbiol. 18, 96–104. https://doi.org/10.1016/j.mib.2014.02.008 (2014).
    CAS  Article  PubMed  Google Scholar 

    42.
    Sun, Z., He, X., Brancaccio, V. F., Yuan, J. & Riedel, C. U. Bifidobacteria exhibit LuxS-dependent autoinducer 2 activity and biofilm formation. PLoS ONE 9, e88260. https://doi.org/10.1371/journal.pone.0088260 (2014).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    43.
    Christiaen, S. E. et al. Autoinducer-2 plays a crucial role in gut colonization and probiotic functionality of Bifidobacterium breve UCC2003. PLoS ONE 9, e98111. https://doi.org/10.1371/journal.pone.0098111 (2014).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    44.
    Yuan, J. et al. A proteome reference map and proteomic analysis of Bifidobacterium longum NCC2705. Mol. Cell. Proteom. 5, 1105–1118. https://doi.org/10.1074/mcp.M500410-MCP200 (2006).
    CAS  Article  Google Scholar 

    45.
    D’Urzo, N. et al. Acidic pH strongly enhances in vitro biofilm formation by a subset of hypervirulent ST-17 Streptococcus agalactiae strains. Appl. Environ. Microbiol. 80, 2176–2185. https://doi.org/10.1128/aem.03627-13 (2014).
    Article  PubMed  PubMed Central  Google Scholar 

    46.
    O’Neill, E. et al. Association between methicillin susceptibility and biofilm regulation in Staphylococcus aureus isolates from device-related infections. J. Clin. Microbiol. 45, 1379–1388. https://doi.org/10.1128/jcm.02280-06 (2007).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    47.
    Hung, D. T., Zhu, J., Sturtevant, D. & Mekalanos, J. J. Bile acids stimulate biofilm formation in Vibrio cholerae. Mol. Microbiol. 59, 193–201. https://doi.org/10.1111/j.1365-2958.2005.04846.x (2006).
    CAS  Article  PubMed  Google Scholar 

    48.
    Maze, A., O’Connell-Motherway, M., Fitzgerald, G. F., Deutscher, J. & van Sinderen, D. Identification and characterization of a fructose phosphotransferase system in Bifidobacterium breve UCC2003. Appl. Environ. Microbiol. 73, 545–553. https://doi.org/10.1128/aem.01496-06 (2007).
    CAS  Article  PubMed  Google Scholar 

    49.
    Lanigan, N., Bottacini, F., Casey, P. G., O’Connell Motherway, M. & van Sinderen, D. Genome-wide search for genes required for bifidobacterial growth under iron-limitation. Front. Microbiol. 8, 964. https://doi.org/10.3389/fmicb.2017.00964 (2017).
    Article  PubMed  PubMed Central  Google Scholar 

    50.
    Ruiz, L., Motherway, M. O., Lanigan, N. & van Sinderen, D. Transposon mutagenesis in Bifidobacterium breve: construction and characterization of a Tn5 transposon mutant library for Bifidobacterium breve UCC2003. PLoS ONE 8, e64699. https://doi.org/10.1371/journal.pone.0064699 (2013).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    51.
    Fanning, S. et al. Bifidobacterial surface-exopolysaccharide facilitates commensal-host interaction through immune modulation and pathogen protection. Proc. Natl. Acad. Sci. USA. 109, 2108–2113. https://doi.org/10.1073/pnas.1115621109 (2012).
    ADS  Article  PubMed  Google Scholar 

    52.
    Alonso-Casajus, N. et al. Glycogen phosphorylase, the product of the glgP Gene, catalyzes glycogen breakdown by removing glucose units from the nonreducing ends in Escherichia coli. J. Bacteriol. 188, 5266–5272. https://doi.org/10.1128/jb.01566-05 (2006).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    53.
    Nocek, B. P., Gillner, D. M., Fan, Y., Holz, R. C. & Joachimiak, A. Structural basis for catalysis by the mono- and dimetalated forms of the dapE-encoded N-succinyl-L, L-diaminopimelic acid desuccinylase. J. Mol. Biol. 397, 617–626. https://doi.org/10.1016/j.jmb.2010.01.062 (2010).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    54.
    Ethapa, T. et al. Multiple factors modulate biofilm formation by the anaerobic pathogen Clostridium difficile. J. Bacteriol. 195, 545–555. https://doi.org/10.1128/jb.01980-12 (2013).
    Article  PubMed  PubMed Central  Google Scholar 

    55.
    Donlan, R. M. Biofilms: microbial life on surfaces. Emerg. Infect. Dis. 8, 881–890. https://doi.org/10.3201/eid0809.020063 (2002).
    Article  PubMed  PubMed Central  Google Scholar 

    56.
    Bottacini, F., Ventura, M., van Sinderen, D. & O’Connell Motherway, M. Diversity, ecology and intestinal function of bifidobacteria. Microbial Cell Fact. https://doi.org/10.1186/1475-2859-13-s1-s4 (2014).
    Article  Google Scholar 

    57.
    Legrand-Defretin, V., Juste, C., Henry, R. & Corring, T. Ion-pair high-performance liquid chromatography of bile salt conjugates: Application to pig bile. Lipids 26, 578–583. https://doi.org/10.1007/bf02536421 (1991).
    CAS  Article  PubMed  Google Scholar 

    58.
    Sanchez, B. et al. Adaptation and response of Bifidobacterium animalis subsp. lactis to bile: a proteomic and physiological approach. Appl. Environ. Microbiol. 73, 6757–6767. https://doi.org/10.1128/aem.00637-07 (2007).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    59.
    Ruas-Madiedo, P., Hernandez-Barranco, A., Margolles, A. & de los Reyes-Gavilan, C. G. A bile salt-resistant derivative of Bifidobacterium animalis has an altered fermentation pattern when grown on glucose and maltose. Appl. Environ. Microbiol. 71, 6564–6570. https://doi.org/10.1128/aem.71.11.6564-6570.2005 (2005).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    60.
    Ruiz, L. et al. The cell-envelope proteome of Bifidobacterium longum in an in vitro bile environment. Microbiology 155, 957–967. https://doi.org/10.1099/mic.0.024273-0 (2009).
    CAS  Article  PubMed  Google Scholar 

    61.
    Wang, G. et al. Functional role of oppA encoding an oligopeptide-binding protein from Lactobacillus salivarius Ren in bile tolerance. J. Ind. Microbiol. Biotechnol. 42, 1167–1174. https://doi.org/10.1007/s10295-015-1634-5 (2015).
    CAS  Article  PubMed  Google Scholar 

    62.
    Lebeer, S. et al. Impact of luxS and suppressor mutations on the gastrointestinal transit of Lactobacillus rhamnosus GG. Appl. Environ. Microbiol. 74, 4711–4718. https://doi.org/10.1128/aem.00133-08 (2008).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    63.
    Wilson, C. M., Aggio, R. B., O’Toole, P. W., Villas-Boas, S. & Tannock, G. W. Transcriptional and metabolomic consequences of LuxS inactivation reveal a metabolic rather than quorum-sensing role for LuxS in Lactobacillus reuteri 100–23. J. Bacteriol. 194, 1743–1746. https://doi.org/10.1128/jb.06318-11 (2012).
    Article  PubMed  PubMed Central  Google Scholar 

    64.
    Rezzonico, F. & Duffy, B. Lack of genomic evidence of AI-2 receptors suggests a non-quorum sensing role for luxS in most bacteria. BMC Microbiol. 8, 154. https://doi.org/10.1186/1471-2180-8-154 (2008).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    65.
    Giddens, S. R. et al. Mutational activation of niche-specific genes provides insight into regulatory networks and bacterial function in a complex environment. Proc. Natl. Acad. Sci. USA 104, 18247. https://doi.org/10.1073/pnas.0706739104 (2007).
    ADS  Article  PubMed  Google Scholar 

    66.
    Thompson, A. P. et al. Glycolysis and pyrimidine biosynthesis are required for replication of adherent–invasive Escherichia coli in macrophages. Microbiology 162, 954–965. https://doi.org/10.1099/mic.0.000289 (2016).
    CAS  Article  PubMed  Google Scholar 

    67.
    Sambrook, J. & Russell, D. Molecular Cloning: A Laboratory Manual 2001 Cold Spring Harbor (Cold Spring Harbor Laboratory Press, New York, 2001).
    Google Scholar 

    68.
    O’Riordan, K. & Fitzgerald, G. F. Molecular characterisation of a 575-kb cryptic plasmid from Bifidobacterium breve NCFB 2258 and determination of mode of replication. FEMS Microbiol. Lett. 174, 285–294. https://doi.org/10.1111/j.1574-6968.1999.tb13581.x (1999).
    CAS  Article  PubMed  Google Scholar 

    69.
    Alessandri, G. et al. Ability of bifidobacteria to metabolize chitin-glucan and its impact on the gut microbiota. Sci. Rep. 9, 5755–5755. https://doi.org/10.1038/s41598-019-42257-z (2019).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    70.
    Duranti, S. et al. Bifidobacterium bifidum and the infant gut microbiota: an intriguing case of microbe-host co-evolution. Environ. Microbiol. 21, 3683–3695. https://doi.org/10.1111/1462-2920.14705 (2019).
    CAS  Article  PubMed  Google Scholar 

    71.
    Fredheim, E. G. et al. Biofilm formation by Staphylococcus haemolyticus. J Clin Microbiol 47, 1172–1180. https://doi.org/10.1128/jcm.01891-08 (2009).
    CAS  Article  PubMed  PubMed Central  Google Scholar  More