More stories

  • in

    Characteristics of pulmonary microvascular structure in postnatal yaks

    AnimalsThe experimental yaks were divided into four groups: 1-day old, 30-days-old, 180-days-old and adult. Three yaks were selected for each group, regardless of sex, and purchased from a local herdsmen in Haiyan County of Qinghai Province. All of the yaks showed a good nutritional status, and appeared healthy with no apparent diseases or conditions. The yaks were sacrificed by exsanguination in a slaughterhouse. The lungs were obtained immediately after the yak had died, and tissue samples were immediately collected from the diaphragmatic lobe of right lungs (to ensure that obvious blood vessels and the trachea were not gathered). The tissue samples were divided into three parts. One part was cut into 1 cm3 sections and fixed with 4% paraformaldehyde (PFA). The other two parts were cut into 1 mm3 pieces; one part was fixed with 2.5% glutaraldehyde, and the other was put into a freezing tube and placed into liquid nitrogen.Ethics statementThis study was approved by the Institutional Animal Care and Use Committee of Qinghai University (Xining, China). All methods were carried out in accordance with the ARRIVE guidelines and the Animal Ethics Procedures and Guidelines of the People’s Republic of China. No local regulations or laws were overlooked. All yaks used in this study were purchased from local farmers.Haematoxylin and eosin stainingLung tissue samples (1 cm3) were fixed in 4% PFA, dehydrated in 30%, 50%, 75%, 95% and 100% ethanol and then treated with xylene before embedding in paraffin. Paraffin-embedded lung tissues were cut into 4 µm sections. The sections were deparaffinized in xylene, and sections were stained either with haematoxylin and eosin (HE) (Y&K Bio, Xi’an, China) or Masson’s trichrome stain, to examine general morphology.ImmunohistochemistryThe unstained, deparaffinized sections were rinsed with Phosphate Buffered Saline with Twen-20 (PBST) 3 times for 5 min each time. Then, endogenous peroxidase was quenched using 3% peroxide-methanol at room temperature in the dark for 25 min, and then the samples were placed on a decolorizing shaking table 3 times, for 5 min each. The slides were then incubated with 3% foetal bovine serum (Sangon Biotech, Shanghai, China) at room temperature for 25 min. The serum was discarded, and rabbit anti-cattle CD34 and rabbit anti-CD34 polyclonal antibodies (Proteintech group, Wuhan, China) diluted in phosphate buffer saline (PBS) were added. CD34 is a transmembrane glycoprotein known as an angiogenesis marker. The sections were incubated in the primary antibodies overnight at 4 °C. Then, the sections were rinsed in Phosphate Buffered Saline with Twen-20 (PBST) (3 × 5 min), goat anti-rabbit IgG was added, and the sections were incubated for 30 min at 37 °C. 3,3-Diaminobenzidin (DAB) was added to the sections to visualise antibody binding, and the sections were washed 3 times in PBST. Haematoxylin was used to counterstain the nucleus prior to the samples being dehydrated and mounted.An Olympus BX51 microscope was used to take photomicrographs of the microstructures, images depict 1000× magnification. Transmission electron microscopy.The TEM lung tissue samples were processed using previously published methods16. Fresh lung samples (1 mm3) were fixed with glutaraldehyde (2.5%, 24 h) and postfixed with osmium tetroxide (1%, 2 h). The samples were dehydrated in a series of increasing concentrations of ethanol and embedded in Epon812. After preparing semithin sections, ultrathin sections were double stained with uranyl acetate and lead citrate. A 10,000× magnification was used to observe and photograph the sections with a JEM 1230 electron microscope (JEOL, Tokyo, Japan) set at 120 kV.Quantitative real-time PCR (qPCR)The gene expression levels in lung tissues from the yaks in the four age groups were analysed using qPCR. Total RNA was isolated with TRIzol® reagent (Invitrogen, CA, USA). cDNA was obtained by reverse transcription of total RNA using the SYBR PrimeScript RT reagent Kit with gDNA Eraser (Perfect Real Time; Takara, Dalian, China). The forward and reverse primers sequences for the qPCR are shown in Table 1. The genes expression levels were detected using TB Green™ Premix Ex Taq™ II (TIi RNaseH Plus; Takara, Dalian, China) according to the manufacturer’s instructions. The 2−ΔΔCT method was used to analyse the relative expression of target genes, and the housekeeping gene β-actin was used for normalization.Table 1 Primer sequences.Full size tableWestern blot analysisEqual amounts of proteins of yak lung tissue in different development stages were harvested. These proteins were separated on 10% polyacrylamide gels and transferred onto polyvinylidene difluoride (PVDF) membranes (Sangon Biotech, Shanghai, China). PVDF membranes were blocked in 10% non-fat (skimmed) milk for 3 h and then incubated in rabbit anti-VEGFA polyclonal antibody (OriGene, Maryland, USA) at 4 °C overnight. The membranes were then incubated with a goat anti-rabbit IgG antibody (Abcam, Cambridge, UK) for 2 h being washed 3 times (10 min / time) with Tris-buffered saline with Twen-20 (TBST; containing 0.1% Twen-20). All antibodies were diluted according to the manufacturer’s instructions. Immunoblots were analysed by autograph using a Gel Doc™ XR + Gel documentation system (BIO-RAD, California, USA).Statistical analysisThe experimental data are showed as the mean ± standard deviation (SD). The differences between the four groups were compared using one-way ANOVA. P values at less than 0.05 were considered significantly different. More

  • in

    Plant-microbe interactions in the phyllosphere: facing challenges of the anthropocene

    1.Kalnay E, Cai M. Impact of urbanization and land-use change on climate. Nature. 2003;423:528–31.CAS 
    PubMed 
    Article 

    Google Scholar 
    2.Archer SDJ, Pointing SB. Anthropogenic impact on the atmospheric microbiome. Nat Microbiol. 2020;5:229–31.CAS 
    PubMed 
    Article 

    Google Scholar 
    3.Powers RP, Jetz W. Global habitat loss and extinction risk of terrestrial vertebrates under future land-use-change scenarios. Nat Clim Change. 2019;9:323–9.Article 

    Google Scholar 
    4.Sandifer PA, Sutton-Grier AE, Ward BP. Exploring connections among nature, biodiversity, ecosystem services, and human health and well-being: Opportunities to enhance health and biodiversity conservation. Ecosyst Serv. 2015;12:1–15.Article 

    Google Scholar 
    5.Jansson JK, Hofmockel KS. Soil microbiomes and climate change. Nat Rev Microbiol. 2020;18:35–46.CAS 
    PubMed 
    Article 

    Google Scholar 
    6.Huttenhower C, Gevers D, Knight R, Abubucker S, Badger JH, Chinwalla AT, et al. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486:207–14.CAS 
    Article 

    Google Scholar 
    7.Banerjee S, Schlaeppi K, van der Heijden MGA. Keystone taxa as drivers of microbiome structure and functioning. Nat Rev Microbiol. 2018;16:567–76.CAS 
    PubMed 
    Article 

    Google Scholar 
    8.Sapp M, Ploch S, Fiore-Donno AM, Bonkowski M, Rose LE. Protists are an integral part of the Arabidopsis thaliana microbiome. Environ Microbiol. 2018;20:30–43.CAS 
    PubMed 
    Article 

    Google Scholar 
    9.Vorholt JA. Microbial life in the phyllosphere. Nat Rev Microbiol. 2012;10:828–40.CAS 
    PubMed 
    Article 

    Google Scholar 
    10.Laforest-Lapointe I, Messier C, Kembel SW. Host species identity, site and time drive temperate tree phyllosphere bacterial community structure. Microbiome. 2016;4:27.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    11.Andrews JH, Harris RF. The ecology and biogeography of microorganisms on plant surfaces. Annu Rev Phytopathol. 2000;38:145–80.Article 

    Google Scholar 
    12.Lugtenberg B, Kamilova F. Plant-growth-promoting Rhizobacteria. Annu Rev Microbiol. 2009;63:541–56.CAS 
    PubMed 
    Article 

    Google Scholar 
    13.Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH. Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol. 2013;11:789–99.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    14.Davison J. Plant beneficial bacteria. Bio/Technol. 1988;6:282–6.CAS 

    Google Scholar 
    15.Schauer S, Kutschera U. A novel growth-promoting microbe, Methylobacterium funariae sp. nov., isolated from the leaf surface of a common moss. Plant Signal Behav. 2011;6:510–5.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    16.Innerebner G, Knief C, Vorholt JA. Protection of arabidopsis thaliana against leaf-pathogenic pseudomonas syringae by sphingomonas strains in a controlled model system. Appl Environ Microbiol. 2011;77:3202–10.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    17.Laforest-Lapointe I, Paquette A, Messier C, Kembel SW. Leaf bacterial diversity mediates plant diversity and ecosystem function relationships. Nature. 2017;546:145–7.CAS 
    PubMed 
    Article 

    Google Scholar 
    18.Koskella B, Meaden S, Crowther WJ, Leimu R, Metcalf CJE. A signature of tree health? Shifts in the microbiome and the ecological drivers of horse chestnut bleeding canker disease. N Phytol. 2017;215:737–46.CAS 
    Article 

    Google Scholar 
    19.Isbell F, Tilman D, Polasky S, Loreau M. The biodiversity-dependent ecosystem service debt. Ecol Lett. 2015;18:119–34.PubMed 
    Article 

    Google Scholar 
    20.Barnosky A, Matzke N, Tomiya S, Wogan G, Swartz B, Quental T, et al. Has the earth’s sixth mass extinction already arrived? Nat Nat. 2011;471:51–7.CAS 
    Article 

    Google Scholar 
    21.Pascual U, Balvanera P, Díaz S, Pataki G, Roth E, Stenseke M, et al. Valuing nature’s contributions to people: the IPBES approach. Curr Opin Environ Sustain. 2017;26–27:7–16.Article 

    Google Scholar 
    22.Cavicchioli R, Ripple WJ, Timmis KN, Azam F, Bakken LR, Baylis M, et al. Scientists’ warning to humanity: microorganisms and climate change. Nat Rev Microbiol. 2019;17:569–86.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    23.Annamalai J, Namasivayam V. Endocrine disrupting chemicals in the atmosphere: Their effects on humans and wildlife. Environ Int. 2015;76:78–97.CAS 
    PubMed 
    Article 

    Google Scholar 
    24.Jumpponen A, Jones KL. Seasonally dynamic fungal communities in the Quercus macrocarpa phyllosphere differ between urban and nonurban environments. N Phytol. 2010;186:496–513.CAS 
    Article 

    Google Scholar 
    25.Imperato V, Kowalkowski L, Portillo-Estrada M, Gawronski SW, Vangronsveld J, Thijs S. Characterisation of the Carpinus betulus L. Phyllomicrobiome in urban and forest areas. Front Microbiol. 2019;10:1110.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    26.Bowers RM, McLetchie S, Knight R, Fierer N. Spatial variability in airborne bacterial communities across land-use types and their relationship to the bacterial communities of potential source environments. ISME J. 2011;5:601–12.CAS 
    PubMed 
    Article 

    Google Scholar 
    27.Lymperopoulou DS, Adams RI, Lindow SE. Contribution of vegetation to the microbial composition of nearby outdoor air. Appl Environ Microbiol. 2016;82:3822–33.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    28.De Kempeneer L, Sercu B, Vanbrabant W, Van Langenhove H, Verstraete W. Bioaugmentation of the phyllosphere for the removal of toluene from indoor air. Appl Microbiol Biotechnol. 2004;64:284–8.PubMed 
    Article 
    CAS 

    Google Scholar 
    29.Hanski I, Hertzen Lvon, Fyhrquist N, Koskinen K, Torppa K, Laatikainen T, et al. Environmental biodiversity, human microbiota, and allergy are interrelated. Proc Natl Acad Sci. 2012;109:8334–9.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    30.Smets W, Wuyts K, Oerlemans E, Wuyts S, Denys S, Samson R, et al. Impact of urban land use on the bacterial phyllosphere of ivy (Hedera sp.). Atmos Environ. 2016;147:376–83.CAS 
    Article 

    Google Scholar 
    31.Laforest-Lapointe I, Messier C, Kembel SW. Tree Leaf Bacterial Community Structure and Diversity Differ along a Gradient of Urban Intensity. mSystems. 2017;2:e00087–17.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    32.Espenshade J, Thijs S, Gawronski S, Bové H, Weyens N, Vangronsveld J. Influence of urbanization on epiphytic bacterial communities of the platanus × hispanica tree leaves in a Biennial Study. Front Microbiol. 2019;10:675.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    33.Wuyts K, Smets W, Lebeer S, Samson R. Green infrastructure and atmospheric pollution shape diversity and composition of phyllosphere bacterial communities in an urban landscape. FEMS Microbiol Ecol 2020;96:fiz173.CAS 
    PubMed 
    Article 

    Google Scholar 
    34.Zhao D, Liu G, Wang X, Daraz U, Sun Q. Abundance of human pathogen genes in the phyllosphere of four landscape plants. J Environ Manag. 2020;255:109933.CAS 
    Article 

    Google Scholar 
    35.Gandolfi I, Canedoli C, Imperato V, Tagliaferri I, Gkorezis P, Vangronsveld J, et al. Diversity and hydrocarbon-degrading potential of epiphytic microbial communities on Platanus x acerifolia leaves in an urban area. Environ Pollut. 2017;220:650–8.CAS 
    PubMed 
    Article 

    Google Scholar 
    36.Weyens N, van der Lelie D, Taghavi S, Vangronsveld J. Phytoremediation: plant–endophyte partnerships take the challenge. Curr Opin Biotechnol. 2009;20:248–54.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    37.Afzal M, Khan QM, Sessitsch A. Endophytic bacteria: prospects and applications for the phytoremediation of organic pollutants. Chemosphere. 2014;117:232–42.CAS 
    PubMed 
    Article 

    Google Scholar 
    38.Siciliano SD, Fortin N, Mihoc A, Wisse G, Labelle S, Beaumier D, et al. Selection of specific endophytic bacterial genotypes by plants in response to soil contamination. Appl Environ Microbiol. 2001;67:2469–75.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    39.Barac T, Taghavi S, Borremans B, Provoost A, Oeyen L, Colpaert JV, et al. Engineered endophytic bacteria improve phytoremediation of water-soluble, volatile, organic pollutants. Nat Biotechnol. 2004;22:583–8.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    40.Sandhu A, Halverson LJ, Beattie GA. Bacterial degradation of airborne phenol in the phyllosphere. Environ Microbiol. 2007;9:383–92.CAS 
    PubMed 
    Article 

    Google Scholar 
    41.Weyens N, Thijs S, Popek R, Witters N, Przybysz A, Espenshade J, et al. The role of plant–microbe interactions and their exploitation for phytoremediation of air pollutants. Int J Mol Sci. 2015;16:25576–604.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    42.Essl F, Dullinger S, Rabitsch W, Hulme PE, Hülber K, Jarošík V, et al. Socioeconomic legacy yields an invasion debt. Proc Natl Acad Sci. 2011;108:203–7.CAS 
    PubMed 
    Article 

    Google Scholar 
    43.Walther G-R, Roques A, Hulme PE, Sykes MT, Pyšek P, Kühn I, et al. Alien species in a warmer world: risks and opportunities. Trends Ecol Evol. 2009;24:686–93.PubMed 
    Article 

    Google Scholar 
    44.Blüthgen N, Menzel F, Blüthgen N. Measuring specialization in species interaction networks. BMC Ecol. 2006;6:9.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    45.Cobian GM, Egan CP, Amend AS. Plant–microbe specificity varies as a function of elevation. ISME J. 2019;13:2778–88.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    46.Bálint M, Bartha L, O’Hara RB, Olson MS, Otte J, Pfenninger M, et al. Relocation, high-latitude warming and host genetic identity shape the foliar fungal microbiome of poplars. Mol Ecol. 2015;24:235–48.PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    47.Vacher C, Cordier T, Vallance J. Phyllosphere fungal communities differentiate more thoroughly than bacterial communities along an elevation gradient. Micro Ecol. 2016;72:1–3.Article 

    Google Scholar 
    48.Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortie CJ, Michalet R, et al. Positive interactions among alpine plants increase with stress. Nature. 2002;417:844–8.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    49.Bever JD. Feeback between plants and their soil communities in an old field. Community Ecol. 1994;75:1965–77.Article 

    Google Scholar 
    50.Bever JD. Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. N Phytol. 2003;157:465–73.Article 

    Google Scholar 
    51.Klironomos JN. Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature. 2002;417:67–70.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    52.Reinhart KO, Callaway RM. Soil biota and invasive plants. N Phytol. 2006;170:445–57.Article 

    Google Scholar 
    53.Callaway RM, Thelen GC, Rodriguez A, Holben WE. Soil biota and exotic plant invasion. Nature. 2004;427:731–3.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    54.Brown CD, Vellend M. Non-climatic constraints on upper elevational plant range expansion under climate change. Proc R Soc B Biol Sci. 2014;281:20141779.Article 

    Google Scholar 
    55.Carteron A, Parasquive V, Blanchard F, Guilbeault‐Mayers X, Turner BL, Vellend M, et al. Soil abiotic and biotic properties constrain the establishment of a dominant temperate tree into boreal forests. J Ecol. 2020;108:931–44.Article 

    Google Scholar 
    56.Williamson M. Biological invasions. 1996. Springer Netherlands.57.Mitchell CE, Power AG. Release of invasive plants from fungal and viral pathogens. Nature. 2003;421:625–7.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    58.Ramirez KS, Snoek LB, Koorem K, Geisen S, Bloem LJ, ten Hooven F, et al. Range-expansion effects on the belowground plant microbiome. Nat Ecol Evol. 2019;3:604–11.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    59.Diez JM, Dickie I, Edwards G, Hulme PE, Sullivan JJ, Duncan RP. Negative soil feedbacks accumulate over time for non-native plant species. Ecol Lett. 2010;13:803–9.PubMed 
    Article 

    Google Scholar 
    60.Lenssen NJL, Schmidt GA, Hansen JE, Menne MJ, Persin A, Ruedy R, et al. Improvements in the GISTEMP uncertainty model. J Geophys Res Atmos. 2019;124:6307–26.Article 

    Google Scholar 
    61.O’brien RD, Lindow SE. Effect of plant species and environmental conditions on ice nucleation activity of pseudomonas syringae on leaves. Appl Environ Microbiol. 1988;54:2281–6.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    62.Klinkert B, Narberhaus F. Microbial thermosensors. Cell Mol Life Sci. 2009;66:2661–76.CAS 
    PubMed 
    Article 

    Google Scholar 
    63.Velásquez AC, Castroverde CDM, He SY. Plant-pathogen warfare under changing climate conditions. Curr Biol CB. 2018;28:R619–R634.PubMed 
    Article 
    CAS 

    Google Scholar 
    64.Compant S, van der Heijden MGA, Sessitsch A. Climate change effects on beneficial plant-microorganism interactions. FEMS Microbiol Ecol. 2010;73:197–214.CAS 
    PubMed 

    Google Scholar 
    65.Cheng YT, Zhang L, He SY. Plant-microbe interactions facing environmental challenge. Cell Host Microbe. 2019;26:183–92.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    66.Guerra CA, Delgado‐Baquerizo M, Duarte E, Marigliano O, Görgen C, Maestre FT, et al. Global projections of the soil microbiome in the Anthropocene. Glob Ecol Biogeogr. 2021;30:987–99.PubMed 
    Article 

    Google Scholar 
    67.Frindte K, Pape R, Werner K, Löffler J, Knief C. Temperature and soil moisture control microbial community composition in an arctic–alpine ecosystem along elevational and micro-topographic gradients. ISME J. 2019;13:2031–43.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    68.Cordier T, Robin C, Capdevielle X, Fabreguettes O, Desprez-Loustau M-L, Vacher C. The composition of phyllosphere fungal assemblages of European beech (Fagus sylvatica) varies significantly along an elevation gradient. N Phytol. 2012;196:510–9.Article 

    Google Scholar 
    69.Tedersoo L, Bahram M, Toots M, Diédhiou AG, Henkel TW, Kjøller R, et al. Towards global patterns in the diversity and community structure of ectomycorrhizal fungi. Mol Ecol. 2012;21:4160–70.PubMed 
    Article 

    Google Scholar 
    70.Gomes T, Pereira JA, Benhadi J, Lino-Neto T, Baptista P. Endophytic and epiphytic phyllosphere fungal communities are shaped by different environmental factors in a Mediterranean ecosystem. Micro Ecol. 2018;76:668–79.Article 

    Google Scholar 
    71.Peñuelas J, Rico L, Ogaya R, Jump AS, Terradas J. Summer season and long-term drought increase the richness of bacteria and fungi in the foliar phyllosphere of Quercus ilex in a mixed Mediterranean forest. Plant Biol Stuttg Ger. 2012;14:565–75.Article 

    Google Scholar 
    72.Rico L, Ogaya R, Terradas J, Peñuelas J. Community structures of N2 -fixing bacteria associated with the phyllosphere of a Holm oak forest and their response to drought. Plant Biol Stuttg Ger. 2014;16:586–93.CAS 
    Article 

    Google Scholar 
    73.Grady KL, Sorensen JW, Stopnisek N, Guittar J, Shade A. Assembly and seasonality of core phyllosphere microbiota on perennial biofuel crops. Nat Commun. 2019;10:1–10.Article 
    CAS 

    Google Scholar 
    74.Redford AJ, Fierer N. Bacterial Succession on the Leaf Surface: A Novel System for Studying Successional Dynamics. Micro Ecol. 2009;58:189–98.Article 

    Google Scholar 
    75.Edwards JA, Santos-Medellín CM, Liechty ZS, Nguyen B, Lurie E, Eason S, et al. Compositional shifts in root-associated bacterial and archaeal microbiota track the plant life cycle in field-grown rice. PLOS Biol. 2018;16:e2003862.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    76.Parmesan C, Yohe G. A globally coherent fingerprint of climate change impacts across natural systems. Nature. 2003;421:37–42.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    77.Zhao C, Liu B, Piao S, Wang X, Lobell DB, Huang Y, et al. Temperature increase reduces global yields of major crops in four independent estimates. Proc Natl Acad Sci. 2017;114:9326–31.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    78.Ray DK, Mueller ND, West PC, Foley JA. Yield trends are insufficient to double global crop production by 2050. PLOS ONE. 2013;8:e66428.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    79.Angel R, Soares MIM, Ungar ED, Gillor O. Biogeography of soil archaea and bacteria along a steep precipitation gradient. ISME J. 2010;4:553–63.PubMed 
    Article 

    Google Scholar 
    80.Kaisermann A, Vries FTde, Griffiths RI, Bardgett RD. Legacy effects of drought on plant–soil feedbacks and plant–plant interactions. N Phytol. 2017;215:1413–24.CAS 
    Article 

    Google Scholar 
    81.Hawkes CV, Kivlin SN, Rocca JD, Huguet V, Thomsen MA, Suttle KB. Fungal community responses to precipitation. Glob Change Biol. 2011;17:1637–45.Article 

    Google Scholar 
    82.Lau JA, Lennon JT. Rapid responses of soil microorganisms improve plant fitness in novel environments. Proc Natl Acad Sci. 2012;109:14058–62.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    83.Sheik CS, Beasley WH, Elshahed MS, Zhou X, Luo Y, Krumholz LR. Effect of warming and drought on grassland microbial communities. ISME J. 2011;5:1692–700.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    84.Bradford MA. Thermal adaptation of decomposer communities in warming soils. Front Microbiol. 2013;4:333.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    85.Li F, Deng J, Nzabanita C, Li Y, Duan T. Growth and physiological responses of perennial ryegrass to an AMF and an Epichloë endophyte under different soil water contents. Symbiosis. 2019;79:151–61.CAS 
    Article 

    Google Scholar 
    86.Ibekwe AM, Ors S, Ferreira JFS, Liu X, Suarez DL, Ma J, et al. Functional relationships between aboveground and belowground spinach (Spinacia oleracea L., cv. Racoon) microbiomes impacted by salinity and drought. Sci Total Environ. 2020;717:137207.CAS 
    PubMed 
    Article 

    Google Scholar 
    87.Prosser JI, Bohannan BJM, Curtis TP, Ellis RJ, Firestone MK, Freckleton RP, et al. The role of ecological theory in microbial ecology. Nat Rev Microbiol. 2007;5:384–92.CAS 
    PubMed 
    Article 

    Google Scholar 
    88.Shoemaker WR, Locey KJ, Lennon JT. A macroecological theory of microbial biodiversity. Nat Ecol Evol. 2017;1:0107.Article 

    Google Scholar 
    89.Ratzke C, Denk J, Gore J. Ecological suicide in microbes. Nat Ecol Evol. 2018;2:867–72.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    90.Shade A, Dunn RR, Blowes SA, Keil P, Bohannan BJM, Herrmann M, et al. Macroecology to unite all life, large and small. Trends Ecol Evol. 2018;33:731–44.PubMed 
    Article 

    Google Scholar 
    91.Grilli J. Macroecological laws describe variation and diversity in microbial communities. Nat Commun. 2020;11:4743.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    92.Knief C, Ramette A, Frances L, Alonso-Blanco C, Vorholt JA. Site and plant species are important determinants of the Methylobacterium community composition in the plant phyllosphere. ISME J. 2010;4:719–28.CAS 
    PubMed 
    Article 

    Google Scholar 
    93.Redford AJ, Bowers RM, Knight R, Linhart Y, Fierer N. The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves: Biogeography of phyllosphere bacterial communities. Environ Microbiol. 2010;12:2885–93.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    94.Remus-Emsermann MNP, Tecon R, Kowalchuk GA, Leveau JHJ. Variation in local carrying capacity and the individual fate of bacterial colonizers in the phyllosphere. ISME J. 2012;6:756–65.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    95.Kembel SW, O’Connor TK, Arnold HK, Hubbell SP, Wright SJ, Green JL. Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest. Proc Natl Acad Sci. 2014;111:13715–20.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    96.Maignien L, DeForce EA, Chafee ME, Eren AM, Simmons SL. Ecological succession and stochastic variation in the assembly of Arabidopsis thaliana phyllosphere communities. mBio. 2014;5:e00682–13.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    97.Wagner MR, Lundberg DS, del Rio TG, Tringe SG, Dangl JL, Mitchell-Olds T. Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. Nat Commun. 2016;7:12151.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    98.Carlström CI, Field CM, Bortfeld-Miller M, Müller B, Sunagawa S, Vorholt JA. Synthetic microbiota reveal priority effects and keystone strains in the Arabidopsis phyllosphere. Nat. Ecol Evol. 2019;3:1445–54.
    Google Scholar 
    99.Lajoie G, Maglione R, Kembel SW. Adaptive matching between phyllosphere bacteria and their tree hosts in a neotropical forest. Microbiome. 2020;8:70.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    100.Massoni J, Bortfeld-Miller M, Jardillier L, Salazar G, Sunagawa S, Vorholt JA. Consistent host and organ occupancy of phyllosphere bacteria in a community of wild herbaceous plant species. ISME J. 2020;14:245–58.CAS 
    PubMed 
    Article 

    Google Scholar 
    101.Lajoie G, Kembel SW. Host neighborhood shapes bacterial community assembly and specialization on tree species across a latitudinal gradient. Ecol Monogr. 2021;91:e01443.Article 

    Google Scholar 
    102.Vellend M. Conceptual synthesis in community ecology. Q Rev Biol. 2010;85:183–206.Article 
    PubMed 

    Google Scholar 
    103.Bernhardt ES, Rosi EJ, Gessner MO. Synthetic chemicals as agents of global change. Front Ecol Environ. 2017;15:84–90.Article 

    Google Scholar  More

  • in

    Preventing spillover as a key strategy against pandemics

    CORRESPONDENCE
    14 September 2021

    Preventing spillover as a key strategy against pandemics

    Neil M. Vora

     ORCID: http://orcid.org/0000-0002-4989-3108

    0
    ,

    Nigel Sizer

    1
    &

    Aaron Bernstein

    2

    Neil M. Vora

    Conservation International, Arlington, Virginia, USA.

    View author publications

    You can also search for this author in PubMed
     Google Scholar

    Nigel Sizer

    Preventing Pandemics at the Source Coalition, Mount Kisco, New York, USA.

    View author publications

    You can also search for this author in PubMed
     Google Scholar

    Aaron Bernstein

    Boston Children’s Hospital, Boston, Massachusetts, USA.

    View author publications

    You can also search for this author in PubMed
     Google Scholar

    Share on Twitter
    Share on Twitter

    Share on Facebook
    Share on Facebook

    Share via E-Mail
    Share via E-Mail

    Download PDF

    Most new infectious diseases result from the spillover of pathogens from animals, particularly wildlife, to people. Spillover prevention should not be dismissed in discussions on how best to address pandemics (see Nature 596, 332–335; 2021).The belief that we are powerless to prevent spillover is, unfortunately, endorsed by many in public health and government. Improved management of farmed animals, regulations on wildlife trade and conservation of tropical forests have all helped to prevent spillover and subsequent outbreaks, as well as boosting greenhouse-gas mitigation and wildlife conservation (see go.nature.com/2uqwx1u). Moreover, preventing spillover is cheap compared with the costs of a single pandemic (A. P. Dobson et al. Science 369, 379–381; 2020).Outbreak containment measures will always be necessary, especially for the most vulnerable people in resource-limited settings, because spillover can never be completely eliminated. But if prioritized alongside post-spillover initiatives, outcomes will be more cost-effective, scientifically informed and equitable.

    Nature 597, 332 (2021)
    doi: https://doi.org/10.1038/d41586-021-02427-4

    Competing Interests
    The authors declare no competing interests.

    Related Articles

    See more letters to the editor

    Subjects

    Diseases

    Policy

    Conservation biology

    Latest on:

    Diseases

    How COVID is derailing the fight against HIV, TB and malaria
    News 10 SEP 21

    Cells of the human intestinal tract mapped across space and time
    Article 08 SEP 21

    Burden and characteristics of COVID-19 in the United States during 2020
    Article 26 AUG 21

    Policy

    Afghanistan: conflict risks local and global health
    Correspondence 14 SEP 21

    Climate science is supporting lawsuits that could help save the world
    News Feature 08 SEP 21

    Indonesia’s science super-agency must earn researchers’ trust
    Editorial 08 SEP 21

    Jobs

    Post-Doctoral Position

    McGuire Research Institute, Inc.
    Richmond, VA, United States

    Postdoctoral Research Associate

    Washington University in St. Louis (WUSTL)
    Saint Louis, MO, United States

    Division Head, General Internal Medicine and Geriatrics, University Health Network and Sinai Health Systems

    University Health Network (UHN), U of T
    Toronto, Ontario, Canada

    Director Protein Science

    Bright Peak Therapeutics
    Basel, Switzerland More

  • in

    Farming with Alternative Pollinators benefits pollinators, natural enemies, and yields, and offers transformative change to agriculture

    The participants of the on-farm trialsThe farmers taking part in the trials own between 0.3 and 40 ha. Most of them were smallholders (less than 2 ha) and used to plant vegetable fields of around 300 m2 per crop. Two out of 233 participating farmers are female, farmers’ age ranges from 24 to 68 years. All farmers learned agriculture from their parents, 70% are literate. Farmers and fields were visited 10–12 times per trial. In 2018, we started with 112 farmer fields, but some farmers did not follow strictly the obligatory agricultural practices (e.g., concerning fertilizer, irrigation, harvest), some lost the entire or parts of fields (e.g., by flood, grazing livestock), therefore all assessments concerning 2018 include 99 farmer fields. In 2019, we started with 136 farmer fields, two farmers did not follow the agreed farming practices, so assessments for 2019 are based on 134 farmer fields.The design of participatory field trialsWe conducted 14 trials in 2018 and 17 in 2019, each trial encompasses five FAP fields and three control fields in neighbouring villages. Minimum distance between FAP fields and between FAP and control fields was two thousand metres for nearly all fields, at least more than one thousand metres. In the mountainous region we used pumpkin, zucchini and faba bean as main crops (two years), in oasis okra and zucchini (two years), faba bean and pumpkin (2019), in the semi-arid region melon, zucchini, pumpkin, eggplant and faba bean (two years) and in the region with adequate rainfall tomato, faba bean, zucchini and eggplant (two years) and pumpkin (2019). The main crops were selected by farmers and agricultural advisors of the respective regions, MHEP by farmers of the respective trials and researchers.Field size was 300 m2 as recommended for smallholders5 with a 75% zone for the main crop in both, FAP and control. Except for okra, the 75% zone had four cultivars with four replications in a randomized system as recommended as enhanced practice by farmers in the pilot project in Morocco27. For okra only two cultivars are available in Morocco and trials used only seeds accessible also for farmers. FAP fields employed the 25% zones for habitat enhancement, whereas control fields had the main crop also in this zone. We used coriander, basil, cumin, dill, anise, celery, sunflower, canola, flax, zucchini, okra, melon, tomato, green pepper, cucumber, Armenian cucumber, eggplant, chia, arugula, watermelon, pumpkin, grass pea, cultivated lupinus, alfalfa, clover, vetch, faba bean and wild lupinus as MHEP, per trial between four and eight different MHEP. As faba bean starts flowering in end of February in Morocco, MHEP were partly forage crops as they flower early. MHEP were seeded in a way that around 2/3 flowered at the same time as the main crop and 1/3 before or after to prolong the foraging season on site for flower visitors. The habitat enhancement zones included also nesting and water support out of local materials, e.g., hollow stems, wood and dry mud with holes.Field managementIn oasis, all fields were irrigated by gravity flow, in the other sites all farmers used drip irrigation. The amount of dung used is based on farmers’ decision and varies per region: semi-arid region 500 kg/300 m2, mountainous region 1000 kg/300 m2, oasis 1500 kg/300 m2 and region with adequate rainfall 3000 kg/300 m2. Soil analysis was conducted for all fields but does not explain the income gaps between FAP and control. Pesticides (mainly neonicotinoids and broad-spectrum insecticides) were prohibited during trials. In some urgent cases with permission of the plant protection specialist, one foliar insecticide application for pest management was accepted when pest density reached the economic threshold.Insect sampling and methods to analyse the dataThe taxa richness of flower visitors was assessed by a combination of transect net samplings and pan trappings. In each field, insects were sampled four times, once before the flowering of the main crop, twice during its flowering and once afterwards. Each sampling took two days for each trial (four fields per day). Two sets of three pan traps (blue, yellow and white) were located in each field at the beginning of the first day of sampling and were collected the second day after 24 h. The samplings in 75% zones consisted of walking along two twenty eight metres transect lines for five min each. In the 25% zones flower visitors were collected once along an 80 m transect line around the 75% zone for ten minutes. The flower visitors were collected and kept separately per MHEP, but the respective time needed was recorded and added to the transect. The insects were collected using both sweep nets and insect vacuums. All flower visitors were collected except Apis mellifera, Bombus terrestris and Xylocopa pubescens that were identified visually on site. The collected insects were first fainted with ethyl acetate and afterwards placed inside killing jars filled with cyanide, afterwards pinned and labelled. Wild bees were identified to the genus level using the most recent key for wild bees in Europe52. The other flower visitors were identified to genus level or to family level. Significance concerning diversity was measured by Wilcoxon test53.In the 75% zones, pest insects, predators and parasitoid wasps were collected four times. Per farmer field, four one-square-metre quadrates were randomly selected, within the quadrates ten randomly selected plants were beaten five times, so in total we used 320 crop samples per trial. In the 25% zones, the beating method was similarly used for each MHEP (five sample plants per MHEP). Specimen were collected in plastic bags and kept in plastic tubes containing 70% ethanol for conservation. Abundance of pests was estimated by counting the number (i) recorded on each sample crop. Pest reduction was calculated by the rate of pest reduction (%) using the following formula: % = (1− AFAP(i) / AControl(i)) × 100, where AFAP (i) is the average of the abundance in the FAP plot; AControl (i) is the average of the abundance in the control plot54.Economic assessmentsThe economic assessments use the same calculation as the pilot projects5,27: the number of fruits was counted and weighed. Investment costs in FAP and control fields are the same in the 75% zones. The income from the 75% zones was assessed by multiplying total weight with market price per kg. The income from the 25% zones of control fields was assessed by total produce weight multiplied by market price per kg; investment costs were deducted. The income of the 25% zone of FAP fields was computed by multiplying total weight with market price per kg of MHEP minus respective investment costs and minus 100 MAD (1.5 person days per FAP field) as calculated labour costs for harvesting MHEP, though in our trials, farmers harvested themselves.SimulationsThe simulation of potential FAP impacts on food security and sparing natural land for pollinator and biodiversity protection is based on following assumptions. Basis is the total production (2016–2017 differentiated per crop; provided by the Moroccan Ministry of Agriculture on request) for faba bean (share of harvested crop with green pods as in the experiments, 105,760 ton in 10,205 ha), zucchini and pumpkin (179,519 ton in 7539 ha), melon (618,588 ton in 20,163 ha), eggplant (52,966 ton in 1885 ha) and tomato (1,293,761 ton in 15,888 ha). We did not include okra due to lack of national production data. For the simulation on potential increase of production through smallholders (≤ 2 ha), we use 13% as share of smallholders in North Africa for vegetable production49. For the simulation of the land-saving potential through smallholders, we used 11% (North Africa, share of smallholders’ land for food crops)55.The formula used for the simulation on the potential FAP impacts on food security (PIFS) is:$${text{PIFS}}, = ,left( {{text{SSP}}*left( {{{1}} – upmu } right)} right), + ,left( {{text{SSP }}*upmu } right){text{ }}*left( {{text{1}}, + ,left( {{text{GFT }}*{text{TE}}} right)} right) – {text{SSP}}$$PIFS: Potential increase in crop production because of FAP (t), SSP: Smallholders’ share of production in (t), GFT: FAP production gain in farm trials (%), µ: the share of smallholder-producers adopting FAP, TE: Technology effectiveness.The GFT employed is 85,2% which represents the average FAP production gain of the vegetables used in the simulation process. For µ we used either 10%, 30% or 50% and for TE we assumed that smallholder-producers gain either 50% or 70% of the total production gain achieved in on-farm trials with smallholder-farmers since farmers will adapt MHEP and their planting to their personal preferences.The formula used for the simulation of potential land saving (PLS):$${text{PLS}} = (({text{SAP}} * {text{PIFS}})/{text{SSP}})-{text{SAP}}$$PLS: Potential land saving in ha, SAP: Smallholders’ area of production in ha. More

  • in

    Analysis of complex trophic networks reveals the signature of land-use intensification on soil communities in agroecosystems

    1.Brussaard, L., Ruiter, P. C. & Brown, G. G. Soil biodiversity for agricultural sustainability. Agric. Ecosyst. Environ. 121, 233–244 (2007).Article 

    Google Scholar 
    2.Nielsen, U. N., Wall, D. H. & Six, J. Soil biodiversity and the environment. Annu. Rev. Environ. Resour. 40, 63–90 (2015).Article 

    Google Scholar 
    3.El Mujtar, V., Muñoz, N., Mc Cormick, B. P., Pulleman, M. & Tittonell, P. Role and management of soil biodiversity for food security and nutrition; where do we stand?. Glob. Food Secur. 20, 132–144 (2019).Article 

    Google Scholar 
    4.Bardgett, R. D. & Putten, W. H. Belowground biodiversity and ecosystem functioning. Nature 515, 505–511 (2014).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    5.Kardol, P. & De Long, J. R. How anthropogenic shifts in plant community composition alter soil food webs. F1000Res 7, 4 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    6.Smith, P. et al. Global change pressures on soils from land-use and management. Glob. Change Biol. 22, 1008–1028 (2016).ADS 
    Article 

    Google Scholar 
    7.Geisen, S. et al. A methodological framework to embrace soil biodiversity. Soil Biol. Biochem. 136, 107536 (2019).CAS 
    Article 

    Google Scholar 
    8.Creamer, R. E. et al. Ecological network analysis reveals the inter-connection between soil biodiversity and ecosystem function as affected by land use across Europe. Appl. Soil. Ecol. 97, 112–124 (2016).Article 

    Google Scholar 
    9.Tsiafouli, M. A. et al. Intensive agriculture reduces soil biodiversity across Europe. Glob. Change Biol. 21, 973–985 (2015).ADS 
    Article 

    Google Scholar 
    10.de Vries, F. T. et al. Soil food web properties explain ecosystem services across European land use systems. PNAS 110, 14296–14301 (2013).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    11.Ponge, J. F. et al. Collembolan communities as bioindicators of land-use intensification. Soil Biol. Biochem. 35, 813–826 (2003).CAS 
    Article 

    Google Scholar 
    12.Postma-Blaauw, M. B., de Goede, R. G. M., Bloem, J., Faber, J. H. & Brussaard, L. Soil biota community structure and abundance under agricultural intensification and extensification. Ecology 91, 460–473 (2010).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    13.Decaëns, T. & Jiménez, J. J. Earthworm communities under an agricultural intensification gradient in Colombia. Plant Soil 240, 133–143 (2002).Article 

    Google Scholar 
    14.Dequiedt, S. et al. Biogeographical patterns of soil molecular microbial biomass as influenced by soil characteristics and management. Globa. Ecol. Biogeogr. 20, 641–652 (2011).Article 

    Google Scholar 
    15.Thomson, B. C. et al. Soil conditions and land-use intensification effects on soil microbial communities across a range of European field sites. Soil Biol. Biochem. 88, 403–413 (2015).CAS 
    Article 

    Google Scholar 
    16.de Graaff, M. A., Hornslein, N., Throop, H., Kardol, P. & van Diepen, L. T. A. Effects of agricultural intensification on soil biodiversity and implications for ecosystem functioning: A meta-analysis. Adv. Agron. 155, 1–44 (2019).Article 

    Google Scholar 
    17.Karimi, B. et al. Biogeography of soil bacterial networks along a gradient of cropping intensity. Sci. Rep. 9, 3812 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    18.Wardle, D. A., Nicholson, K. S., Bonner, K. I. & Yeates, G. W. Effects of agricultural intensification on soil-associated arthropod population dynamics, community structure, diversity and temporal variability over a seven-year period. Soil Biol. Biochem. 31, 1691–1706 (1999).CAS 
    Article 

    Google Scholar 
    19.Gossner, M. M. et al. Land-use intensification causes multitrophic homogenization of grassland communities. Nature 540, 266–269 (2016).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    20.Valiente-Banuet, A. et al. Beyond species loss: The extinction of ecological interactions in a changing world. Funct. Ecol. 29, 299–307 (2015).Article 

    Google Scholar 
    21.Freilich, M. A., Wieters, E., Broitman, B. R., Marquet, P. A. & Navarrete, S. A. Species co-occurrence networks: Can they reveal trophic and non-trophic interactions in ecological communities?. Ecology 99, 690–699 (2018).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    22.Gray, C. et al. FORUM: Ecological networks: The missing links in biomonitoring science. J. Appl. Ecol. 51, 1444–1449 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    23.Evans, D., Kitson, J., Lunt, D., Straw, N. & Pocock, M. Merging DNA metabarcoding and ecological network analysis to understand and build resilient terrestrial ecosystems. Funct. Ecol. 30, 1904–1916 (2016).Article 

    Google Scholar 
    24.Ruppert, K. M., Kline, R. J. & Rahman, M. S. Past, present, and future perspectives of environmental DNA (eDNA) metabarcoding: A systematic review in methods, monitoring, and applications of global eDNA. Glob. Ecol. Conserv. 17, 00547 (2019).
    Google Scholar 
    25.Taberlet, P., Coissac, E., Hajibabaei, M. & Rieseberg, L. H. Environmental DNA. Mol. Ecol. 21, 1789–1793 (2012).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    26.Vacher, C. et al. Chapter one—Learning ecological networks from next-generation sequencing data. Adv. Ecol. Res. 54, 1–39 (2016).Article 

    Google Scholar 
    27.Poelen, J. H., Simons, J. D. & Mungall, C. J. Global biotic interactions: An open infrastructure to share and analyze species-interaction datasets. Ecol. Inform. 24, 148–159 (2014).Article 

    Google Scholar 
    28.Nguyen, N. H. et al. FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol. 20, 241–248 (2016).Article 

    Google Scholar 
    29.Dopheide, A. et al. Rarity is a more reliable indicator of land-use impacts on soil invertebrate communities than other diversity metrics. Elife 9, e52787 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    30.García-Callejas, D., Molowny-Horas, R. & Araújo, M. B. Multiple interactions networks: Towards more realistic descriptions of the web of life. Oikos 127, 5–22 (2018).Article 

    Google Scholar 
    31.Delmas, E. et al. Analysing ecological networks of species interactions. Biol. Rev. 94, 16–36 (2019).Article 

    Google Scholar 
    32.Morrison, B. M. L., Brosi, B. J. & Dirzo, R. Agricultural intensification drives changes in hybrid network robustness by modifying network structure. Ecol. Lett. 23, 359–369 (2020).PubMed 
    Article 

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

    Google Scholar 
    34.Thakur, M. P. & Wright, A. J. Environmental filtering, niche construction, and trait variability: The missing discussion. Trends Ecol. Evol. 32, 884–886 (2017).PubMed 
    Article 

    Google Scholar 
    35.Xue, L. et al. Long term effects of management practice intensification on soil microbial community structure and co-occurrence network in a non-timber plantation. For. Ecol. Manag. 459, 117805 (2020).Article 

    Google Scholar 
    36.Felipe-Lucia, M. R. et al. Land-use intensity alters networks between biodiversity, ecosystem functions, and services. PNAS https://doi.org/10.1073/pnas.2016210117 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    37.Heemsbergen, D. A. et al. Biodiversity effects on soil processes explained by interspecific functional dissimilarity. Science 306, 1019–1020 (2004).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    38.Erdozain, M. et al. Metabarcoding of storage ethanol vs. conventional morphometric identification in relation to the use of stream macroinvertebrates as ecological indicators in forest management. Ecol. Indic. 101, 173–184 (2019).CAS 
    Article 

    Google Scholar 
    39.Moore, J. C., McCann, K., Setälä, H. & De Ruiter, P. C. Top-down is bottom-up: Does predation in the rhizosphere regulate aboveground dynamics?. Ecology 84, 846–857 (2003).Article 

    Google Scholar 
    40.Wollrab, S., Diehl, S. & De Roos, A. M. Simple rules describe bottom-up and top-down control in food webs with alternative energy pathways. Ecol. Lett. 15, 935–946 (2012).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    41.de Vries, F. T. & Wallenstein, M. D. Below-ground connections underlying above-ground food production: A framework for optimising ecological connections in the rhizosphere. J. Ecol. 105, 913–920 (2017).Article 

    Google Scholar 
    42.de Vries, F. T. & Caruso, T. Eating from the same plate? Revisiting the role of labile carbon inputs in the soil food web. Soil Biol. Biochem. 102, 4–9 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    43.Bramon Mora, B., Gravel, D., Gilarranz, L. J., Poisot, T. & Stouffer, D. B. Identifying a common backbone of interactions underlying food webs from different ecosystems. Nat. Commun. 9, 2603 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

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

    Google Scholar 
    45.Malik, A. A. et al. Land-use driven change in soil pH affects microbial carbon cycling processes. Nat. Commun. 9, 3591 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    46.Jia, Y. & Whalen, J. K. Functional redundancy and phylogenetic niche conservatism in the soil microbial community. Pedosphere 30, 18–24 (2020).ADS 
    Article 

    Google Scholar 
    47.Bush, A. et al. DNA metabarcoding reveals metacommunity dynamics in a threatened boreal wetland wilderness. Proc. Natl. Acad. Sci. 117, 8539–8545 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    48.Blüthgen, N. et al. A quantitative index of land-use intensity in grasslands: Integrating mowing, grazing and fertilization. Basic Appl. Ecol. 13, 207–220 (2012).Article 

    Google Scholar 
    49.Ruiz-Martinez, I., Marraccini, E., Debolini, M. & Bonari, E. Indicators of agricultural intensity and intensification: A review of the literature. Ital. J. Agron. 10, 74–84 (2015).Article 

    Google Scholar 
    50.Taberlet, P., Bonin, A., Zinger, L. & Coissac, E. Environmental DNA: For Biodiversity Research and Monitoring (OUP Oxford, Oxford, 2018).Book 

    Google Scholar 
    51.Taberlet, P. et al. Soil sampling and isolation of extracellular DNA from large amount of starting material suitable for metabarcoding studies. Mol. Ecol. 21, 1816–1820 (2012).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    52.Boyer, F. et al. obitools: A unix-inspired software package for DNA metabarcoding. Mol. Ecol. Resour. 16, 176–182 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    53.Zinger, L. et al. Extracellular DNA extraction is a fast, cheap and reliable alternative for multi-taxa surveys based on soil DNA. Soil Biol. Biochem. 96, 16–19 (2016).CAS 
    Article 

    Google Scholar 
    54.Compson, Z. G. et al. Chapter two—Linking DNA metabarcoding and text mining to create network-based biomonitoring tools: A case study on boreal wetland macroinvertebrate communities. Adv. Ecol. Res. 59, 33–74 (2018).Article 

    Google Scholar 
    55.G.B.I.F. GBIF backbone taxonomy. (2017).56.Allesina, S. & Pascual, M. Food web models: A plea for groups. Ecol. Lett. 12, 652–662 (2009).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    57.Gauzens, B., Thébault, E., Lacroix, G. & Legendre, S. Trophic groups and modules: Two levels of group detection in food webs. J. R. Soc. Interface 12, 20141176 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    58.Makiola, A. et al. Key questions for next-generation biomonitoring. Front. Environ. Sci. 7, 197 (2020).Article 

    Google Scholar 
    59.Nowicki, K. & Snijders, T. A. B. Estimation and prediction for stochastic block structures. J. Am. Stat. Assoc. 96, 1077–1087 (2001).MATH 
    Article 

    Google Scholar 
    60.Biernacki, C., Celeux, G. & Govaert, G. Assessing a mixture model for clustering with the integrated completed likelihood. IEEE Trans. Pattern Anal. Mach. Intell. 22, 719–725 (2000).Article 

    Google Scholar 
    61.Compson, Z. G. et al. Network-based biomonitoring: Exploring freshwater food webs with stable isotope analysis and DNA metabarcoding. Front. Ecol. Evol. 7, 395 (2019).Article 

    Google Scholar 
    62.Ohlmann, M. et al. Diversity indices for ecological networks: A unifying framework using Hill numbers. Ecol. Lett. 22, 737–747 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    63.Gauzens, B., Legendre, S., Lazzaro, X. & Lacroix, G. Intermediate predation pressure leads to maximal complexity in food webs. Oikos 125, 595–603 (2016).Article 

    Google Scholar 
    64.Lau, M. K., Borrett, S. R., Baiser, B., Gotelli, N. J. & Ellison, A. M. Ecological network metrics: Opportunities for synthesis. Ecosphere 8, 01900 (2017).Article 

    Google Scholar  More

  • in

    Terrestrial mesopredators did not increase after top-predator removal in a large-scale experimental test of mesopredator release theory

    1.Barnosky, A. D. et al. Has the Earth’s sixth mass extinction already arrived?. Nature 471(7336), 51–57 (2011).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    2.Ripple, W. J. et al. Status and ecological effects of the world’s largest carnivores. Science 343, 151–163 (2014).CAS 
    Article 

    Google Scholar 
    3.Haswell, P. M., Kusak, J. & Hayward, M. W. Large carnivore impacts are context-dependent. Food Webs 12, 3–13. https://doi.org/10.1016/j.fooweb.2016.02.005 (2017).Article 

    Google Scholar 
    4.Barbosa, P. & Castellanos, I. Ecology of Predator–Prey Interactions (Oxford University Press, 2005).
    Google Scholar 
    5.Terborgh, J. & Estes, J. A. Trophic Cascades: Predator, Prey, and the Changing Dynamics of Nature (Island Press, 2010).
    Google Scholar 
    6.Estes, J. A. et al. Trophic downgrading of planet earth. Science 333, 301–306 (2011).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    7.Crooks, K. R. & Soulé, M. E. Mesopredator release and avifaunal extinctions in a fragmented system. Nature 400, 563–566 (1999).ADS 
    CAS 
    Article 

    Google Scholar 
    8.Ritchie, E. G. & Johnson, C. N. Predator interactions, mesopredator release and biodiversity conservation. Ecol. Lett. 12(9), 982–998. https://doi.org/10.1111/j.1461-0248.2009.01347.x (2009).Article 
    PubMed 

    Google Scholar 
    9.Jachowski, D. S. et al. Identifying mesopredator release in multi-predator systems: A review of evidence from North America. Mamm. Rev. 50, 367–381. https://doi.org/10.1111/mam.12207 (2020).Article 

    Google Scholar 
    10.Letnic, M., Ritchie, E. G. & Dickman, C. R. Top predators as biodiversity regulators: The dingo Canis lupus dingo as a case study. Biol. Rev. 87(2), 390–413. https://doi.org/10.1111/j.1469-185X.2011.00203.x (2012).Article 
    PubMed 

    Google Scholar 
    11.Glen, A. S. & Dickman, C. R. Complex interactions among mammalian carnivores in Australia, and their implications for wildlife management. Biol. Rev. 80(3), 387–401 (2005).PubMed 
    Article 

    Google Scholar 
    12.Allen, B. L. et al. Can we save large carnivores without losing large carnivore science?. Food Webs. 12, 64–75 (2017).Article 

    Google Scholar 
    13.Allen, B. L. & Leung, K.-P. The (non)effects of lethal population control on the diet of Australian dingoes. PLoS ONE 9(9), e108251. https://doi.org/10.1371/journal.pone.0108251 (2014).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    14.Wallach, A. D. Australia should enlist dingoes to control invasive species. The Conversation 2014. https://theconversation.com/australia-should-enlist-dingoes-to-control-invasive-species-24807. Accessed 26 March, 2014.15.Letnic, M. & Feit, B. Like cats and dogs: dingoes can keep feral cats in check. The Conversation. 2019. https://theconversation.com/like-cats-and-dogs-dingoes-can-keep-feral-cats-in-check-114748. Accessed 4 April 2019.16.Newsome, T. Thinking big gives top predators the competitive edge. The Conversation 2017. https://theconversation.com/thinking-big-gives-top-predators-the-competitive-edge-78106. Accessed 24 May 2017.17.Johnson, C. & VanDerWal, J. Evidence that dingoes limit the abundance of a mesopredator in eastern Australian forests. J Appl Ecol. 46, 641–646 (2009).Article 

    Google Scholar 
    18.Rolls, E. C. They All Ran Wild: The Animals and Plants that Plague Australia (Angus & Robertson Publishers, 1969).
    Google Scholar 
    19.Balme, J., O’Connor, S. & Fallon, S. New dates on dingo bones from Madura Cave provide oldest firm evidence for arrival of the species in Australia. Sci. Rep. 8(1), 9933. https://doi.org/10.1038/s41598-018-28324-x (2018).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    20.Fleming, P. J. S., Allen, B. L. & Ballard, G. Seven considerations about dingoes as biodiversity engineers: The socioecological niches of dogs in Australia. Aust. Mammal. 34(1), 119–131 (2012).Article 

    Google Scholar 
    21.Corbett, L. K. The Dingo in Australia and Asia 2nd edn. (J.B. Books, South Australia, 2001).
    Google Scholar 
    22.Fleming, P. J. S. et al. Management of wild canids in Australia: Free-ranging dogs and red foxes. In Carnivores of Australia: Past, Present and Future (eds Glen, A. S. & Dickman, C. R.) 105–149 (CSIRO Publishing, 2014).
    Google Scholar 
    23.Doherty, T. S. et al. Impacts and management of feral cats Felis catus in Australia. Mamm. Rev. 42, 83–97 (2017).Article 

    Google Scholar 
    24.Brook, L. A., Johnson, C. N. & Ritchie, E. G. Effects of predator control on behaviour of an apex predator and indirect consequences for mesopredator suppression. J. Appl. Ecol. 49(6), 1278–1286. https://doi.org/10.1111/j.1365-2664.2012.02207.x (2012).Article 

    Google Scholar 
    25.Letnic, M., Koch, F., Gordon, C., Crowther, M. & Dickman, C. Keystone effects of an alien top-predator stem extinctions of native mammals. Proc. R. Soc. B Biol. Sci. 276, 3249–3256 (2009).Article 

    Google Scholar 
    26.Wallach, A. D., Johnson, C. N., Ritchie, E. G. & O’Neill, A. J. Predator control promotes invasive dominated ecological states. Ecol. Lett. 13, 1008–1018 (2010).PubMed 

    Google Scholar 
    27.Leo, V., Reading, R. P., Gordon, C. & Letnic, M. Apex predator suppression is linked to restructuring of ecosystems via multiple ecological pathways. Oikos 128, 630–639. https://doi.org/10.1111/oik.05546 (2019).Article 

    Google Scholar 
    28.Johnson, C. Australia’s Mammal Extinctions: A 50,000 Year History (Cambridge University Press, 2006).
    Google Scholar 
    29.Read, J. L. & Scoleri, V. Ecological implications of reptile mesopredator release in arid South Australia. J. Herpetol. 49(1), 64–69. https://doi.org/10.1670/13-208 (2015).Article 

    Google Scholar 
    30.Sutherland, D. R., Glen, A. S. & de Tores, P. J. Could controlling mammalian carnivores lead to mesopredator release of carnivorous reptiles?. Proc. R. Soc. B 278(1706), 641–648. https://doi.org/10.1098/rspb.2010.2103 (2010).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    31.Davis, N. E. et al. Interspecific and geographic variation in the diets of sympatric carnivores: Dingoes/wild dogs and red foxes in south-eastern Australia. PLoS ONE 10(3), e0120975. https://doi.org/10.1371/journal.pone.0120975 (2015).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    32.Paltridge, R. The diets of cats, foxes and dingoes in relation to prey availability in the Tanami Desert, Northern Territory. Wildl. Res. 29, 389–403 (2002).Article 

    Google Scholar 
    33.Cupples, J. B., Crowther, M. S., Story, G. & Letnic, M. Dietary overlap and prey selectivity among sympatric carnivores: Could dingoes suppress foxes through competition for prey?. J. Mammal. 92(3), 590–600. https://doi.org/10.1644/10-MAMM-A-164.1 (2011).Article 

    Google Scholar 
    34.Glen, A. S., Pennay, M., Dickman, C. R., Wintle, B. A. & Firestone, K. B. Diets of sympatric native and introduced carnivores in the Barrington Tops, eastern Australia. Aust. Ecol. 36(3), 290–296. https://doi.org/10.1111/j.1442-9993.2010.02149.x (2011).Article 

    Google Scholar 
    35.Moseby, K. E., Neilly, H., Read, J. L. & Crisp, H. A. Interactions between a top order predator and exotic mesopredators in the Australian rangelands. Int. J. Ecol. 2012; Article ID 250352.36.Allen, B. L. & Fleming, P. J. S. Reintroducing the dingo: The risk of dingo predation to threatened vertebrates of western New South Wales. Wildl. Res. 39(1), 35–50 (2012).Article 

    Google Scholar 
    37.Glen, A. S. & Woodman, A. P. What Impact Does Altering Dingo Populations Have on Trophic Structure? (Environmental Evidence Australia, 2013).
    Google Scholar 
    38.Allen, B. L., Allen, L. R. & Leung, K.-P. Interactions between two naturalised invasive predators in Australia: Are feral cats suppressed by dingoes?. Biol. Invasions 17, 761–776. https://doi.org/10.1007/s10530-014-0767-1 (2015).Article 

    Google Scholar 
    39.Arthur, A. D., Catling, P. C. & Reid, A. Relative influence of habitat structure, species interactions and rainfall on the post-fire population dynamics of ground-dwelling vertebrates. Aust. Ecol. 37(8), 958–970 (2013).Article 

    Google Scholar 
    40.Claridge, A. W., Cunningham, R. B., Catling, P. C. & Reid, A. M. Trends in the activity levels of forest-dwelling vertebrate fauna against a background of intensive baiting for foxes. For. Ecol. Manag. 260(5), 822–832. https://doi.org/10.1016/j.foreco.2010.05.041 (2010).Article 

    Google Scholar 
    41.Stobo-Wilson, A. M. et al. Habitat structural complexity explains patterns of feral cat and dingo occurrence in monsoonal Australia. Divers. Distrib. 247, 108638. https://doi.org/10.1111/ddi.13065 (2020).Article 

    Google Scholar 
    42.Pavey, C. R., Eldridge, S. R. & Heywood, M. Population dynamics and prey selection of native and introduced predators during a rodent outbreak in arid Australia. J. Mammal. 89(3), 674–683 (2008).Article 

    Google Scholar 
    43.Greenville, A. C., Wardle, G. M., Tamayo, B. & Dickman, C. R. Bottom-up and top-down processes interact to modify intraguild interactions in resource-pulse environments. Oecologia 175(4), 1349–1358. https://doi.org/10.1007/s00442-014-2977-8 (2014).ADS 
    Article 
    PubMed 

    Google Scholar 
    44.Allen, B. L. et al. Does lethal control of top-predators release mesopredators? A re-evaluation of three Australian case studies. Ecol. Manag. Restor. 15(3), 191–195. https://doi.org/10.1111/emr.12118 (2014).Article 

    Google Scholar 
    45.Allen, B. L. et al. As clear as mud: A critical review of evidence for the ecological roles of Australian dingoes. Biol. Conserv. 159, 158–174 (2013).Article 

    Google Scholar 
    46.Hayward, M. W. & Marlow, N. Will dingoes really conserve wildlife and can our methods tell?. J. Appl. Ecol. 51(4), 835–838. https://doi.org/10.1111/1365-2664.12250 (2014).Article 

    Google Scholar 
    47.Newsome, T. M., Greenville, A. C., Letnic, M., Ritchie, E. G. & Dickman, C. R. The case for a dingo reintroduction in Australia remains strong: A reply to Morgan et al., 2016. Food Webs https://doi.org/10.1016/j.fooweb.2017.02.001 (2017).Article 

    Google Scholar 
    48.Letnic, M., Crowther, M. S., Dickman, C. R. & Ritchie, E. Demonising the dingo: How much wild dogma is enough?. Curr. Zool. 57(5), 668–670 (2011).Article 

    Google Scholar 
    49.Glen, A. S. Enough dogma: Seeking the middle ground on the role of dingoes. Curr. Zool. 58(6), 856–858 (2012).Article 

    Google Scholar 
    50.Johnson, C. N. et al. Experiments in no-impact control of dingoes: Comment on Allen et al. 2013. Front. Zool. 11, 17 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    51.Nimmo, D. G., Watson, S. J., Forsyth, D. M. & Bradshaw, C. J. A. Dingoes can help conserve wildlife and our methods can tell. J. Appl. Ecol. 52(2), 281–285. https://doi.org/10.1111/1365-2664.12369 (2015).Article 

    Google Scholar 
    52.Allen, B. L. et al. Top-predators as biodiversity regulators: Contemporary issues affecting knowledge and management of dingoes in Australia. In Biodiversity Enrichment in a Diverse World. Chapter 4 (ed. Lameed, G. A.) 85–132 (InTech Publishing, 2012).
    Google Scholar 
    53.Platt, J. R. Strong inference: Certain systematic methods of scientific thinking may produce much more rapid progress than others. Science 146(3642), 347–353 (1964).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    54.Caughley, G. Analysis of Vertebrate Populations (Wiley, 1977).
    Google Scholar 
    55.Krebs, C. J. Ecology: The Experimental Analysis of Distribution and Abundance 6th edn. (Benjamin-Cummings Publishing, 2008).
    Google Scholar 
    56.Hone, J. Wildlife Damage Control (CSIRO Publishing, 2007).Book 

    Google Scholar 
    57.Fox, G. A., Negrete-Yankelevich, S. & Sosa, V. J. Ecological Statistics: Contemporary Theory and Application (Oxford University Press, 2015).MATH 
    Book 

    Google Scholar 
    58.Kershaw, K. A. Quantitative and Dynamic Ecology (Edward Arnold Publishers, 1969).
    Google Scholar 
    59.Li, J. C. R. Introduction to Statistical Inference (Edwards Bos Distributors, 1957).Book 

    Google Scholar 
    60.Quinn, G. P. & Keough, M. J. Experimental Design and Data Analysis for Biologists (Cambridge University Press, 2002).Book 

    Google Scholar 
    61.Shadish, W. R., Cook, T. D. & Campbell, D. T. Experimental and Quasi-experimental Designs for Generalized Casual Inference 2nd edn. (Houghton, Mifflin and Company, 2002).
    Google Scholar 
    62.Underwood, A. J. Experiments in Ecology (Cambridge University Press, 1997).
    Google Scholar 
    63.Allen, B. L., Allen, L. R., Engeman, R. M. & Leung, L.K.-P. Intraguild relationships between sympatric predators exposed to lethal control: Predator manipulation experiments. Front. Zool. 10, 39 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    64.Allen, B. L., Allen, L. R., Engeman, R. M. & Leung, L.K.-P. Sympatric prey responses to lethal top-predator control: Predator manipulation experiments. Front. Zool. 11, 56 (2014).Article 

    Google Scholar 
    65.Eldridge, S. R., Shakeshaft, B. J. & Nano, T. J. The impact of wild dog control on cattle, native and introduced herbivores and introduced predators in central Australia. Final report to the Bureau of Rural Sciences. Alice Springs: Parks and Wildlife Commission of the Northern Territory; 2002.66.Kennedy, M., Phillips, B., Legge, S., Murphy, S. & Faulkner, R. Do dingoes suppress the activity of feral cats in northern Australia?. Austral Ecol. 37(1), 134–139 (2012).Article 

    Google Scholar 
    67.Allen, B. L., Allen, L. R., Engeman, R. M. & Leung, L. K.-P. Reply to the criticism by Johnson et al. (2014) on the report by Allen et al. (2013). Front. Zool. 2014. http://www.frontiersinzoology.com/content/11/1/7/comments#1982699. Accessed 1st June 2014.68.Newsome, T. M. et al. Resolving the value of the dingo in ecological restoration. Restor. Ecol. 23(3), 201–208. https://doi.org/10.1111/rec.12186 (2015).Article 

    Google Scholar 
    69.Glen, A. S., Dickman, C. R., Soulé, M. E. & Mackey, B. G. Evaluating the role of the dingo as a trophic regulator in Australian ecosystems. Austral Ecol. 32(5), 492–501 (2007).Article 

    Google Scholar 
    70.Mitchell, B. & Balogh, S. Monitoring techniques for vertebrate pests: wild dogs. Orange: NSW Department of Primary Industries, Bureau of Rural Sciences; 2007.71.Letnic, M. & Koch, F. Are dingoes a trophic regulator in arid Australia? A comparison of mammal communities on either side of the dingo fence. Austral Ecol. 35(2), 267–175 (2010).Article 

    Google Scholar 
    72.Contos, P. & Letnic, M. Top-down effects of a large mammalian carnivore in arid Australia extend to epigeic arthropod assemblages. J. Arid Environ. (in press). https://doi.org/10.1016/j.jaridenv.2019.03.002.73.Mills, C. H., Wijas, B., Gordon, C. E., Lyons, M., Feit, A., Wilkinson, A., et al. Two alternate states: Shrub, bird and mammal assemblages differ on either side of the Dingo Barrier Fence. Aust Zool. (in press). https://doi.org/10.7882/az.2021.005.74.Engeman, R. M., Allen, L. R. & Allen, B. L. Study design concepts for inferring functional roles of mammalian top predators. Food Webs. 12, 56–63 (2017).Article 

    Google Scholar 
    75.Kennedy, M. S., Kreplins, T. L., O’Leary, R. A. & Fleming, P. A. Responses of dingo (Canis familiaris) populations to landscape-scale baiting. Food Webs. (in press). https://doi.org/10.1016/j.fooweb.2021.e00195.76.Allen, L. R. Is landscape-scale wild dog control best practice?. Australas. J. Environ. Manag. 24(1), 5–15 (2017).Article 

    Google Scholar 
    77.Ballard, G., Fleming, P. J. S., Meek, P. D. & Doak, S. Aerial baiting and wild dog mortality in south-eastern Australia. Wildl. Res. 47(2), 99–105. https://doi.org/10.1071/WR18188 (2020).Article 

    Google Scholar 
    78.Smith, D. & Allen, B. L. Habitat use by yellow-footed rock-wallabies in predator exclusion fences. J. Arid Environ. (in press).79.Smith, D., King, R. & Allen, B. L. Impacts of exclusion fencing on target and non-target fauna: A global review. Biol. Rev. 95(6), 1590–1606 (2020).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    80.Smith, D., Waddell, K. & Allen, B. L. Expansion of vertebrate pest exclusion fencing and its potential benefits for threatened fauna recovery in Australia. Animals 10, 1550 (2020).PubMed Central 
    Article 
    PubMed 

    Google Scholar 
    81.Clark, P., Clark, E. & Allen, B. L. Sheep, dingoes and kangaroos: New challenges and a change of direction 20 years on. In Advances in Conservation Through Sustainable Use of Wildlife (eds Baxter, G. et al.) 173–178 (University of Queensland, 2018).
    Google Scholar 
    82.Allen, L. R. The Impact of Wild Dog Predation and Wild Dog Control on Beef Cattle: Large-Scale Manipulative Experiments Examining the Impact of and Response to Lethal Control (LAP Lambert Academic Publishing, 2013).
    Google Scholar 
    83.Allen, L. R. Demographic and functional responses of wild dogs to poison baiting. Ecol. Manag. Restor. 16(1), 58–66 (2015).Article 

    Google Scholar 
    84.Eldridge, S. R., Bird, P. L., Brook, A., Campbell, G., Miller, H. A., Read, J. L., et al. The effect of wild dog control on cattle production and biodiversity in the South Australian arid zone: Final report. Port Augusta, South Australia: South Australian Arid Lands Natural Resources Management Board; 2016.85.Fancourt, B. A., Cremasco, P., Wilson, C. & Gentle, M. N. Do introduced apex predators suppress introduced mesopredators? A multiscale spatiotemporal study of dingoes and feral cats in Australia suggests not. J. Appl. Ecol. 56(12), 2584–2595. https://doi.org/10.1111/1365-2664.13514 (2019).Article 

    Google Scholar 
    86.Allen, B. L., Engeman, R. M. & Allen, L. R. Wild dogma I: An examination of recent “evidence” for dingo regulation of invasive mesopredator release in Australia. Curr. Zool. 57(5), 568–583 (2011).Article 

    Google Scholar 
    87.Allen, L. R. & Engeman, R. M. Evaluating and validating abundance monitoring methods in the absence of populations of known size: Review and application to a passive tracking index. Environ. Sci. Pollut. Res. 22, 2907–2915. https://doi.org/10.1007/s11356-014-3567-3 (2014).Article 

    Google Scholar 
    88.Caughley, G. Analysis of Vertebrate Populations, reprinted with corrections. (Wiley, 1980).
    Google Scholar 
    89.Wysong, M. L. et al. Space use and habitat selection of an invasive mesopredator and sympatric, native apex predator. Mov. Ecol. 8(1), 18. https://doi.org/10.1186/s40462-020-00203-z (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    90.Ritchie, E. G. et al. Ecosystem restoration with teeth: What role for predators?. Trends Ecol. Evol. 27(5), 265–271 (2012).PubMed 
    Article 

    Google Scholar 
    91.Letnic, M. Stop poisoning dingoes to protect native animals. University of New South Wales, Sydney, available at http://newsroom.unsw.edu.au/news/science/stop-poisoning-dingoes-protect-native-mammals. Accessed 1 April 2014: UNSW Newsroom; 2014.92.Ritchie, E. G. The world’s top predators are in decline, and it’s hurting us too. The Conversation. 2014. http://theconversation.com/the-worlds-top-predators-are-in-decline-and-its-hurting-us-too-21830. Accessed 10 January 2014.93.Brown, J. S., Laundre, J. W. & Gurung, M. The ecology of fear: Optimal foraging, game theory, and trophic interactions. J. Mammal. 80, 385–399 (1999).Article 

    Google Scholar 
    94.Laundré, J. W. et al. The landscape of fear: The missing link to understand top-down and bottom-up controls of prey abundance?. Ecology 95(5), 1141–1152. https://doi.org/10.1890/13-1083.1 (2014).Article 
    PubMed 

    Google Scholar 
    95.Haswell, P. M., Jones, K. A., Kusak, J. & Hayward, M. W. Fear, foraging and olfaction: How mesopredators avoid costly interactions with apex predators. Oecologia https://doi.org/10.1007/s00442-018-4133-3 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    96.Colman, N. J., Gordon, C. E., Crowther, M. S. & Letnic, M. Lethal control of an apex predator has unintended cascading effects on forest mammal assemblages. Proc. R. Soc. B Biol. Sci. 281(1782), 20133094. https://doi.org/10.1098/rspb.2013.3094 (2014).CAS 
    Article 

    Google Scholar 
    97.Sheriff, M. J., Peacor, S., Hawlena, D. & Thaker, M. Non-consumptive predator effects on prey population size: A dearth of evidence. J. Anim. Ecol. 89, 1302–1316. https://doi.org/10.1111/1365-2656.13213 (2020).Article 
    PubMed 

    Google Scholar 
    98.Fleming, P. J. S. et al. Roles for the Canidae in food webs reviewed: Where do they fit?. Food Webs. 12(Supplement C), 14–34. https://doi.org/10.1016/j.fooweb.2017.03.001 (2017).Article 

    Google Scholar 
    99.Wang, Y. & Fisher, D. Dingoes affect activity of feral cats, but do not exclude them from the habitat of an endangered macropod. Wildl. Res. 39, 611–620 (2012).Article 

    Google Scholar 
    100.Hayward, M. W. et al. Ecologists need robust survey designs, sampling and analytical methods. J. Appl. Ecol. 52(2), 286–290. https://doi.org/10.1111/1365-2664.12408 (2015).Article 

    Google Scholar 
    101.Johnson, C. N. & Ritchie, E. The dingo and biodiversity conservation: response to Fleming et al. (2012). Aust. Mammal. 35(1), 8–14 (2013).Article 

    Google Scholar 
    102.Wallach, A. D. & O’Neill, A. J. Threatened species indicate hot-spots of top-down regulation. Anim. Biodivers. Conserv. 32(2), 127–133 (2009).
    Google Scholar 
    103.Feit, B., Feit, A. & Letnic, M. Apex predators decouple population dynamics between mesopredators and their prey. Ecosystems. (in press). https://doi.org/10.1007/s10021-019-00360-2.104.Gordon, C. E., Moore, B. D. & Letnic, M. Temporal and spatial trends in the abundances of an apex predator, introduced mesopredator and ground-nesting bird are consistent with the mesopredator release hypothesis. Biodivers. Conserv. https://doi.org/10.1007/s10531-017-1309-9 (2017).Article 

    Google Scholar 
    105.Letnic, M. et al. Does a top predator suppress the abundance of an invasive mesopredator at a continental scale?. Glob. Ecol. Biogeogr. 20(2), 343–353 (2011).Article 

    Google Scholar 
    106.Rees, J. D., Kingsford, R. T. & Letnic, M. Changes in desert avifauna associated with the functional extinction of a terrestrial top predator. Ecography 42(1), 67–76. https://doi.org/10.1111/ecog.03661 (2019).Article 

    Google Scholar 
    107.Allen, B. L. et al. Large carnivore science: Non-experimental studies are useful, but experiments are better. Food Webs 13, 49–50 (2017).Article 

    Google Scholar 
    108.Allen, B. L., Engeman, R. M. & Allen, L. R. Wild dogma II: The role and implications of wild dogma for wild dog management in Australia. Curr. Zool. 57(6), 737–740 (2011).Article 

    Google Scholar 
    109.Fleming, P. J. S., Allen, B. L. & Ballard, G. Cautionary considerations for positive dingo management: A response to the Johnson and Ritchie critique of Fleming et al. (2012). Aust Mammal. 35(1), 15–22 (2013).Article 

    Google Scholar 
    110.Allen, B. L. Did dingo control cause the elimination of kowaris through mesopredator release effects? A response to Wallach and O’Neill (2009). Anim. Biodivers. Conserv. 33(2), 1–4 (2010).
    Google Scholar 
    111.Woinarski, J. C. Z. et al. Reading the black book: The number, timing, distribution and causes of listed extinctions in Australia. Biol. Conserv. 239, 108261. https://doi.org/10.1016/j.biocon.2019.108261 (2019).Article 

    Google Scholar 
    112.Kearney, S. G., Cawardine, J., Reside, A. E., Fisher, D., Maron, M., Doherty, T. S., et al. The threats to Australia’s imperilled species and implications for a national conservation response. Pac. Conserv. Biol. (in press). https://doi.org/10.1071/PC18024.113.Burbidge, A. A. & McKenzie, N. L. Patterns in the modern decline of Western Australia’s vertebrate fauna: Causes and conservation implications. Biol. Conserv. 50, 143–198 (1989).Article 

    Google Scholar 
    114.Lunney, D. Causes of the extinction of native mammals of the western division of New South Wales: An ecological interpretation of the nineteenth century historical record. Rangel. J. 23(1), 44–70 (2001).Article 

    Google Scholar 
    115.Cremona, T., Crowther, M. S. & Webb, J. K. High mortality and small population size prevents population recovery of a reintroduced mesopredator. Anim. Conserv. 20, 555–563. https://doi.org/10.1111/acv.12358 (2017).Article 

    Google Scholar 
    116.Bannister, H. L., Lynch, C. E. & Moseby, K. E. Predator swamping and supplementary feeding do not improve reintroduction success for a threatened Australian mammal, Bettongia lesueur. Aust. Mammal. 38, 177–187 (2016).Article 

    Google Scholar 
    117.Mori, E. et al. Spatiotemporal mechanisms of coexistence in an European mammal community in a protected area of southern Italy. J. Zool. 310(3), 232–245. https://doi.org/10.1111/jzo.12743 (2020).Article 

    Google Scholar 
    118.Saggiomo, L. Mesopredator Release and Competitive Exclusion: A Global Review and Potential for European Carnivores [Masters] (Alma Mater Studiorum University, 2014).
    Google Scholar 
    119.Gigliotti, L. C. et al. Context dependency of top-down, bottom-up and density-dependent influences on cheetah demography. J. Anim. Ecol. 89, 449–459. https://doi.org/10.1111/1365-2656.13099 (2020).Article 
    PubMed 

    Google Scholar 
    120.Cozzi, G. et al. Fear of the dark or dinner by moonlight? Reduced temporal partitioning among Africa’s large carnivores. Ecology 93(12), 2590–2599. https://doi.org/10.1890/12-0017.1 (2012).Article 
    PubMed 

    Google Scholar 
    121.Rafiq, K. et al. Spatial and temporal overlaps between leopards (Panthera pardus) and their competitors in the African large predator guild. J. Zool. 311(4), 246–259. https://doi.org/10.1111/jzo.12781 (2020).Article 

    Google Scholar 
    122.Comley, J., Joubert, C. J., Mgqatsa, N. & Parker, D. M. Lions do not change rivers: Complex African savannas preclude top-down forcing by large predators. J. Nat. Conserv. 56, 125844 (2020).Article 

    Google Scholar 
    123.Allen, M. L., Peterson, B. & Krofel, M. No respect for apex carnivores: Distribution and activity patterns of honey badgers in the Serengeti. Mamm. Biol. 89, 90–94. https://doi.org/10.1016/j.mambio.2018.01.001 (2018).Article 

    Google Scholar 
    124.Vitekere, K. et al. Dynamic in species estimates of carnivores (leopard cat, red fox, and north Chinese leopard): A multi-year assessment of occupancy and coexistence in the Tieqiaoshan Nature Reserve, Shanxi Province, China. Animals 10(8), 1333. https://doi.org/10.3390/ani10081333 (2020).Article 
    PubMed Central 
    PubMed 

    Google Scholar 
    125.Brodie, J. F. & Giordano, A. Lack of trophic release with large mammal predators and prey in Borneo. Biol. Conserv. 63, 58–67. https://doi.org/10.1016/j.biocon.2013.01.003 (2013).Article 

    Google Scholar 
    126.Lahkar, D., Ahmed, M. F., Begum, R. H., Das, S. K. & Harihar, A. Inferring patterns of sympatry among large carnivores in Manas National Park—A prey-rich habitat influenced by anthropogenic disturbances. Anim. Conserv. (in press). https://doi.org/10.1111/acv.12662.127.Gehrt, S. D. & Prange, S. Interference competition between coyotes and raccoons: A test of the mesopredator release hypothesis. Behav. Ecol. 18(1), 204–214 (2007).Article 

    Google Scholar 
    128.Dias, D. M., Massara, R. L., de Campos, C. B. & Rodrigues, F. H. G. Feline predator–prey relationships in a semi-arid biome in Brazil. J. Zool. (in press). https://doi.org/10.1111/jzo.12647.129.Foster, V. C. et al. Jaguar and puma activity patterns and predator–prey interactions in four Brazilian biomes. Biotropica 45(3), 373–379. https://doi.org/10.1111/btp.12021 (2013).Article 

    Google Scholar 
    130.Allen, L. R. Best practice baiting: Dispersal and seasonal movement of wild dogs (Canis lupus familiaris). Technical highlights: Invasive plant and animal research 2008–09. Brisbane: QLD Department of Employment, Economic Development and Innovation; 2009. 61–62.131.Fleming, P., Corbett, L., Harden, R. & Thomson, P. Managing the impacts of dingoes and other wild dogs. Bomford M, editor. Canberra: Bureau of Rural Sciences; 2001.132.Thomas, L. et al. Distance software: Design and analysis of distance sampling surveys for estimating population size. J. Appl. Ecol. 47, 5–14 (2010).PubMed 
    Article 

    Google Scholar 
    133.Ruette, S., Stahl, P. & Albaret, M. Applying distance-sampling methods to spotlight counts of red foxes. J. Appl. Ecol. 40, 32–43 (2003).Article 

    Google Scholar 
    134.Engeman, R. Indexing principles and a widely applicable paradigm for indexing animal populations. Wildl. Res. 32(3), 202–210 (2005).Article 

    Google Scholar 
    135.R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing; 2020. More

  • in

    Plant biodiversity assessment through pollen DNA metabarcoding in Natura 2000 habitats (Italian Alps)

    Biodiversity assessment through DNA metabarcodingOur analysis detected 160 Operational Taxonomic Units (OTUs) with 12,007,712 sequenced reads, 222,370 ± 41,954 (sd) reads per sample, for a total of 54 sequenced samples. The rarefaction curves showed good sequencing effort for the samples (Supplementary Figure S1) which were rarefied to the least count among samples corresponding to 135,443 reads. Twenty OTUs, (7.2% of the total), were assigned to taxa not relevant to our work (mainly to mosses and ferns during the periods October 2014–March 2015 and July–October 2015). From the remaining OTUs, 108 (88% of the reads) were taxonomically assigned to 32 families of vascular plants (68 identified taxa) (Table 2, Supplementary Table S1) and 32 OTUs (4.8% of the reads) remained unidentified either because of low sequence identity and/or query coverage percentage or the absence of any sequence classification result, even when compared to the complete ‘Nucleotide’ Genbank database. The results of the taxonomic assignment to vascular plants are presented in Supplementary Table S1. The OTU sequences were assigned to plant taxa with at least 95% identity and coverage, from which 70% of the OTUs had ≥ 98% sequence identity with the assigned taxa. The positive control of the DNA extraction, Corylus avellana pollen, was correctly identified after HTS. From the 19 negative controls included in the extraction plate, one negative control was selected for sequencing, the only one with sufficient amplicon concentration (2 ng μl−1). In this sample two OTUs were detected (263,649 reads), both assigned to Quercus spp. and contributing  More

  • in

    Tea plantations and their importance as host plants and hot spots for epiphytic cryptogams

    1.Namita, P., Mukesh, R. & Vijay, K. J. Camellia Sinensis (Green Tea): A review. Glob. J. Pharmacol. 6(2), 52–59 (2012).
    Google Scholar 
    2.Chang, K. World Tea Production and Trade. Current and Future Development (FAO, Rome, 2015).
    Google Scholar 
    3.Chang, K. & Brattlof, M. World Tea Production and Trade. Current and Future Development (FAO, 2015).
    Google Scholar 
    4.Kochlamazashvili, I. & Kakulia, N. The Georgian Tea Sector: A Value Chain Study. ISET Policy Institute. Study prepared in the framework of ENPARD project Cooperation for Rural Prosperity in Georgia (2015).5.Lesica, P., McCune, B., Cooper, S. V. & Hong, W. S. Differences in lichen and bryophyte communities between old-growth and managed second-growth forests in the Svan Valley Montana. Can. J. Bot. 69, 1745–1755 (1991).Article 

    Google Scholar 
    6.Nowak, A., Plášek, V., Nobis, M. & Nowak, S. Epiphytic communities of open habitats in the Western Tian-Shan Mts (Middle Asia: Kyrgyzstan). Cryptog. Bryol. 37(4), 415–433 (2016).Article 

    Google Scholar 
    7.Rhoades, F. M. Nonvascular epiphytes in forest canopies: Worldwide distribution, abundance and ecological roles. In Forest Canopies (eds. Lowman, M.D. & Nadkarni, N. M.) 353–408 (1995).8.Haines, W. P. & Renwick, J. A. A. Bryophytes as food: Comparative consumption and utilization of mosses by a generalist insect herbivore. Entomol Exp Appl. 133, 296–306. https://doi.org/10.1111/j.1570-7458.2009.00929.x (2009).Article 

    Google Scholar 
    9.Kuřavová, K. et al. Is feeding on mosses by groundhoppers in the genus Tetrix (Insecta: Orthoptera) opportunistic or selective?. Arthropod-Plant Int. 11, 35–43. https://doi.org/10.1007/s11829-016-9461-9 (2017).Article 

    Google Scholar 
    10.Matuszkiewicz, W. Przewodnik do Oznaczania Zbiorowisk Roślinnych Polski (Wyd Nauk, PWN, 2001).
    Google Scholar 
    11.Krestov, P. V. Forest vegetation of easternmost Russia (Russian Far East). In Forest Vegetation of Northeast Asia (eds Kolbek, J. et al.) 93–180 (Springer, 2003).Chapter 

    Google Scholar 
    12.Kuznetsov, O. Topology-ecological classification of mire vegetation in the Republic of Karelia (Russia). In Biodiversity and Conservation of Boreal Nature. Proceedings of the 10 years anniversary symposium of the Nature Reserve Friendship (eds Heikkilä, R. & Lindholm, T.) 117–123 (Elsevier, 2003).
    Google Scholar 
    13.Černý, T. Phytosociological Study of Selected Critical Thermophilous Vegetation Complexes in the Czech Republic. A thesis submitted for the degree of Doctor of Philosophy in the Department of Botany Faculty of Sciences, Charles University (2007).14.Chytrý, M. et al. A modern analogue of the Pleistocene steppe-tundra ecosystem in southern Siberia. Boreas 48, 36–56 (2019).Article 

    Google Scholar 
    15.Wolski, G. J. & Kruk, A. Determination of plant communities based on bryophytes: The combined use of Kohonen artificial neural network and indicator species analysis. Ecol. Indic 113, 106160. https://doi.org/10.1016/j.ecolind.2020.106160 (2020).Article 

    Google Scholar 
    16.Benzing, D. Vulnerabilities of tropical forests to climate change: The significance of resident epiphytes. Clim. Change 39, 519–540 (1998).Article 

    Google Scholar 
    17.Gustafsson, L., Fiskesjö, A., Ingelög, T., Petterson, B. & Thor, G. Factors of importance to some lichen species of deciduous broad-leaved woods in southern Sweden. Lichenologist 24, 255–266 (1992).Article 

    Google Scholar 
    18.Frahm, J. P. Ecology of bryophytes along altitudinal and latitudinal gradients in Chile. Trop. Bryol. 21, 67–79 (2002).
    Google Scholar 
    19.Číhal, L., Kaláb, O. & Plášek, V. Modeling the distribution of rare and interesting moss species of the family Orthotrichaceae (Bryophyta) in Tajikistan and Kyrgyzstan. Acta Soc. Bot. Pol. 86(2), 3543. https://doi.org/10.5586/asbp.3543 (2017).Article 

    Google Scholar 
    20.Łubek, A., Kukwa, M., Czortek, P. & Jaroszewicz, B. Impact of Fraxinus excelsior dieback on biota of ash-associated lichen epiphytes at the landscape and community level. Biodivers. Conserv. 29, 431–450. https://doi.org/10.1007/s10531-019-01890-w (2020).Article 

    Google Scholar 
    21.Łubek, A., Kukwa, M., Jaroszewicz, B. & Czortek, P. Identifying mechanisms shaping lichen functional diversity in a primeval forest. For. Ecol. Manag. 475, 118434. https://doi.org/10.1016/j.foreco.2020.118434 (2020).Article 

    Google Scholar 
    22.Barkman, J. J. Phytosociology and Ecology of Cryptogamic Epiphytes. Including a Taxonomic Survey and Description of Their Vegetation Units in Europe, Van Gorcum, Comp (N. V Assen, 1958).
    Google Scholar 
    23.Green, T. G. A. & Lange, O. L. Photosynthesis in poikilohydric plants: A comparison of lichens and bryophytes. In Ecophysiology of Photosynthesis (eds Schulze, E.-D. & Caldwell, M. M.) 319–341 (Springer-Verlag, 1995).Chapter 

    Google Scholar 
    24.Scheidegger, C., Wolseley, P. A. & Landolt, R. Towards conservation of lichens. Forest. Snow Landsc. Res. 75, 285–433 (2000).
    Google Scholar 
    25.Tønsberg, T. & Høiland, K. A study of the macrolichen flora on the sand-dune areas on Lista, SW Norway. Nor. J. Bot. 27, 131–134 (1980).
    Google Scholar 
    26.Thiet, R. K., Doshas, A. & Smith, S. M. Effects of biocrusts and lichen-moss mats on plant productivity in a US sand dune ecosystem. Plant Soil 377(1), 235–244 (2014).CAS 
    Article 

    Google Scholar 
    27.Vaz, A. S., Marques, J. & Honrado, J. P. Patterns of lichen diversity in coastal sand-dunes of northern Portugal. Bot. Complut. 38, 89–96 (2014).Article 

    Google Scholar 
    28.Antoninka, A., Bowker, M. A., Reed, S. C. & Doherty, K. Production of greenhouse-grown biocrust mosses and associated cyanobacteria to rehabilitate dryland soil function. Restor. Ecol. 24(3), 324–335 (2016).Article 

    Google Scholar 
    29.Jüriado, I., Kämärä, M.-L. & Oja, E. Environmental factors and ground disturbance affecting the composition of species and functional traits of ground layer lichens on grey dunes and dune heaths of Estonia. Nord. J. Bot. 34(2), 244–255 (2016).Article 

    Google Scholar 
    30.Balogh, R. et al. Mosses and lichens in dynamics of acidic sandy grasslands: Specific response to grazing exclosure. Acta Biol. Plant. Agriensis 5(1), 30 (2017).
    Google Scholar 
    31.Concostrina-Zubiri, L., Arenas, J. M., Martínez, I. & Escudero, A. Unassisted establishment of biological soil crusts on dryland road slopes. Web Ecol. 19(1), 39–51 (2019).Article 

    Google Scholar 
    32.Kubiak, D. & Oszyczka, P. Non-forested vs forest environments: The effect of habitat conditionson host tree parameters and the occurrence of associated epiphytic lichens. Fungal Ecol. 47, 100957 (2020).Article 

    Google Scholar 
    33.Gradstein, S. R. & Sporn, S. G. Land-use change and epiphytic bryophyte diversity in the Tropics. Nova Hedwigia 138, 311–323 (2010).
    Google Scholar 
    34.Guevara, S., Purata, S. E. & Van der Maarel, E. The role of remnant forest trees in tropical secondary succession. Vegetatio 66, 77–84 (1986).
    Google Scholar 
    35.Sillett, S. C., Gradstein, S. R. & Griffin, D. Bryophyte diversity of Ficus tree crowns from cloud forest and pasture in Costa Rica. Bryologist 98(2), 251–260 (1995).Article 

    Google Scholar 
    36.Werner, F., Homeier, J. & Gradstein, S. R. Diversity of vascular epiphytes on isolated remnant trees in the montane forest belt of southern Ecuador. Ecotropica 11, 21–40 (2005).
    Google Scholar 
    37.Lara, F., Garilleti, R. & Mazimpaka, V. Orthotrichum karoo (Orthotrichaceae), a new species with hyaline-awned leaves from southwestern Africa. Bryologist 112(1), 194–201 (2009).Article 

    Google Scholar 
    38.Lara, F. & Mazimpaka, V. Ma´s sobre la presencia de Orthotrichum acuminatum en la Península Ibérica. Cryptog. Bryol. Lichenol. 13(4), 349–354 (1992).
    Google Scholar 
    39.Garilleti, R., Lara, F. & Mazimpaka, V. Orthotrichum anodon (Orthotrichaceae, Bryopsida), a new species from California, and its relationships with other Orthotricha sharing puckered capsule mouths. Bryologist 109(2), 188–196 (2006).Article 

    Google Scholar 
    40.Hallingbäck, T. & Hodgetts, N. Mosses Liverworts and Hornworts. Status survey and conservation action plan for bryophytes (Cambridge University Press, 2000).
    Google Scholar 
    41.Belinchón, R., Martínez, I., Escudero, A., Aragón, G. & Valladares, F. Edge effects on epiphytic communities in a Mediterranean Quercus pyrenaica forest. J. Veg. Sci. 18, 81–90. https://doi.org/10.1111/j.1654-1103.2007.tb02518.x (2007).Article 

    Google Scholar 
    42.Boudreault, C., Gauthier, S. & Bergeron, Y. Epiphytic lichens and bryophytes on Populus Tremuloides along a chronosequence in the Southwestern Boreal Forest of Quebec, Canada. Bryologist 103, 725–738. https://doi.org/10.1639/0007-2745(2000)103[0725:ELABOP]2.0.CO;2 (2009).Article 

    Google Scholar 
    43.Rambo, T. Structure and composition of corticolous epiphyte communities in a Sierra Nevada old-growth mixed-conifer forest. Bryologist 113, 55–71. https://doi.org/10.1639/0007-2745-113.1.55 (2010).Article 

    Google Scholar 
    44.Plášek, V., Nowak, A., Nobis, M., Kusza, G. & Kochanowska, K. Effect of 30 years of road traffic abandonment on epiphytic moss diversity. Environ. Monit. Assess. 186, 8943–8959. https://doi.org/10.1007/s10661-014-4056-3 (2014).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    45.Skoupá, Z., Ochyra, R., Guo, S. L., Sulayman, M. & Plášek, V. Distributional novelties for Lewinskya, Nyholmiella and Orthotrichum (Orthotrichaceae) in China. Herzogia 30, 58–73. https://doi.org/10.13158/heia.30.1.2017.58 (2017).Article 

    Google Scholar 
    46.Skoupá, Z., Ochyra, R., Guo, S.-L., Sulayman, M. & Plášek, V. Three remarkable additions of Orthotrichum species (Orthotrichaceae) to the moss flora of China. Herzogia 31, 88–100. https://doi.org/10.13158/099.031.0105 (2018).Article 

    Google Scholar 
    47.Gradstein, R. et al. Bryophytes of Mount Patuha, West Java, Indonesia. Reinwardtia 13(2), 107–123 (2010).
    Google Scholar 
    48.Saat, A., Talib, M. S., Harun, N., Hamzah, Z. & Wood, A. K. Spatial variability of arsenic and heavy metals in a highland tea plantation using lichens and mosses as bio-monitors. Asian J. Nat. Appl. Sci. 5(1), 10–21 (2016).
    Google Scholar 
    49.Fick, S. E. & Hijmans, R. J. WorldClim 2: New 1km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37(12), 4302–4315 (2017).Article 

    Google Scholar 
    50.Wirth, V. Ökologische Zeigerwerte von Flechten. Herzogia 23(2), 229–248 (2010).Article 

    Google Scholar 
    51.Ellenberger, H. et al. Zeigerwerte von Planzen in Mitteleuropa. Scr. Geobot. 18, 1–248 (1991).
    Google Scholar 
    52.Smith, C. W. et al. The Lichens of Great Britain and Ireland 1046 (British Lichen Society, 2009).
    Google Scholar 
    53.Hodgetts, N. et al. An annotated checklist of bryophytes of Europe, Macaronesia and Cyprus. J. Bryol. 42(1), 1–116. https://doi.org/10.1080/03736687.2019.1694329 (2020).Article 

    Google Scholar 
    54.Pancho, J. V. Some bryophytes in tea plantations, Pagilaran Central Java. Biotrop. Bull. 11, 279–282 (1979).
    Google Scholar 
    55.Tan, B. C. et al. Mosses of Gunung Halimun National Park, West Java, Indonesia. Reinwardtia 12, 205–214 (2006).
    Google Scholar 
    56.Ohsawa, M. Weeds of tea plantations. In Biology and Ecology of Weeds. Geobotany Vol. 2 (eds Holzner, W. & Numata, M.) (Springer, 1982).
    Google Scholar 
    57.Gradstein, R. et al. Bryophytes of Mount Patuha, West Java, Indonesia. Reinwardtia 13, 107–123 (2010).
    Google Scholar 
    58.Whitelaw, M. & Burton, M. A. S. Diversity and distribution of epiphytic bryophytes on Bramley’s Seedling trees in East of England apple orchards. Glob. Ecol. Conserv. 4, 380–387. https://doi.org/10.1016/j.gecco.2015.07.014 (2015).Article 

    Google Scholar 
    59.Söderström, L. Bryophytes and decaying wood – a comparison between manager and natural forest. Holarc. Ecol. 14, 121–130 (1991).
    Google Scholar 
    60.Cieśliński, S. et al. Relikty lasu puszczańskiego, In Białowieski Park Narodowy (1921–1996) w badaniach geobotanicznych. Phytocoenosis, 8 (N.S.), Seminarium Geobotanicum (ed. Faliński, J. B.) 4, 47–64 (1996).61.Vanderpoorten, A., Engels, P. & Sotiaux, A. Trends in diversity and abundance of obligate epiphytic bryophytes in a highly managed landscape. Ecography 27, 567–576 (2004).Article 

    Google Scholar 
    62.Ódor, P., van Dort, K., Aude, E., Heilmann-Clausen, J. & Christensen, M. Diversity and composition of dead wood inhabiting bryophyte communities in European beech forest. Biol. Soc. Esp. Briol. 26–27, 85–102 (2005).
    Google Scholar 
    63.Friedel, A., Oheimb, G. V., Dengler, J. & Härdtle, W. Species diversity and species composition of epiphytic bryophytes and lichens: A comparison of managed and unmanaged beech forests in NE Germany. Feddes Repert. 117(1–2), 172–185 (2006).Article 

    Google Scholar 
    64.Wolski, G. J. Siedliskowe Uwarunkowania Występowania Mszaków w Rezerwatach Przyrody Chroniących Jodłę Pospolitą w Polsce Środkowej (Praca doktorska wykonana w Katedrze Geobotaniki i Ekologii Roślin UŁ, 2013).
    Google Scholar 
    65.Fudali, E. & Wolski, G. J. Ecological diversity of bryophytes on tree trunks in protected forests (a case study from Central Poland). Herzogia 28(1), 91–107 (2015).Article 

    Google Scholar 
    66.Shi, X.-M. et al. Epiphytic bryophytes as bio-indicators of atmospheric nitrogen deposition in a subtropical montane cloud forest: Response patterns, mechanism, and critical load. Environ. Pollut. 229, 932–941. https://doi.org/10.1016/j.envpol.2017.07.077 (2017).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    67.Cornelissen, J. H. C. & Gradstein, S. R. On the occurrence of bryophytes and macrolichens in different lowland rain forest types of Mabura Hill, Guyana. Trop. Bryol. 3, 29–35. https://doi.org/10.11646/bde.3.1.4 (1990).Article 

    Google Scholar 
    68.Lyons, B., Nadkarni, N. M. & North, M. P. Spatial distribution and succession of epiphytes on Tsuga heterophylla (western hemlock) in an old-growth Douglas-fir forest. Can. J. Bot. 78(7), 957–968. https://doi.org/10.1139/cjb-78-7-957 (2000).Article 

    Google Scholar 
    69.Cornelissen, J. H. C. & Steege, H. T. Distribution and ecology of epiphytic bryophytes and lichens in dry evergreen forest of Guyana. J. Trop. Ecol. 5, 131–150. https://doi.org/10.1017/S0266467400003400 (1989).Article 

    Google Scholar 
    70.Woods, C. L., Cardelús, C. L., Dewalt, S. J. & Piper, F. Microhabitat associations of vascular epiphytes in a wet tropical forest canopy. J. Ecol. 103(2), 421–430. https://doi.org/10.1111/1365-2745.12357 (2015).Article 

    Google Scholar 
    71.Sporn, S. G., Bos, M. M., Kessler, M. & Gradstein, S. R. Vertical distribution of epiphytic bryophytes in an Indonesian rainforest. Biodivers. Conserv. 19(3), 745–760. https://doi.org/10.1007/s10531-009-9731-2 (2010).Article 

    Google Scholar 
    72.Czerepko, J. et al. How sensitive are epiphytic and epixylic cryptogams as indicators of forest naturalness? Testing bryophyte and lichen predictive power in stands under different management regimes in the Białowieża forest. Ecol. Indic. 125, 107532. https://doi.org/10.1016/j.ecolind.2021.107532 (2021).Article 

    Google Scholar 
    73.Putna, S. & Mězaka, A. Preferences of epiphytic bryophytes for forest stand and substrate in North-East Latvia. Folia Cryptog. Estonica 51, 75–83 (2014).Article 

    Google Scholar 
    74.Manakyan, V. A. Results of bryological studies in Armenia. Arctoa 5, 15–33 (1995).Article 

    Google Scholar 
    75.Redfearn, P. L., Tan, B. C. & He, S. A newly updated and annotated checklist of Chines mosses. J. Hattori Bot. Lab. 79, 163–357 (1996).
    Google Scholar 
    76.Kürschner, H. Bryophyte Flora of the Arabian Peninsula and Socotra. Bryophytorum Bibliotheca (JCramer in der Gebrüder Borntraeger Verlagsbuchhandlung, 2000).
    Google Scholar 
    77.Higuchi, M. & Nishimura, N. Mosses of Pakistan. J. Hattori Bot. Lab. 93, 273–291 (2003).
    Google Scholar 
    78.Ignatov, M. S., Afonina, O. M. & Ignatova, E. A. Check-list of mosses of East Europe and North Asia. Arctoa 15, 1–130. https://doi.org/10.15298/arctoa.15.01 (2006).Article 

    Google Scholar 
    79.Sabovljević, M. et al. Check-list of the mosses of SE Europe. Phytol. Balcan. 14(2), 207–244 (2008).
    Google Scholar 
    80.Dandotiya, D., Govindapyari, H., Suman, S. & Uniyal, P. L. Checklist of the bryophytes of India. Arch. Bryol. 88, 71–72 (2011).
    Google Scholar 
    81.Hodgetts, N. G. Checklist and Country Status of European bryophytes—Towards a New Red List for Europe. Irish Wildlife Manuals, No. 84. (National Parks and Wildlife Service, Department of Arts, Heritage and the Gaeltacht, 2011). https://www.hdl.handle.net/2262/73373.82.Kürschner, H. & Frey, W. Liverworts, Mosses and Hornworts of Southwest Asia (Marchantiophyta, Bryophyta, Anthoceroptophyta). Nova Hedwigia 139, 179–180 (2011).
    Google Scholar 
    83.Suzuki, T. A revised new catalog of the mosses of Japan. Hattoria 7, 9–223. https://doi.org/10.18968/hattoria.7.0_9 (2016).Article 

    Google Scholar 
    84.Kürschner, H. & Frey, W. Liverworts, mosses and hornworts of Afghanistan—our present knowledge. Acta Mus. Siles. Sci. Natur. 68, 11–24 (2019).
    Google Scholar 
    85.Brotherus, V. F. Enumeratio muscorum Caucasi. Acta Soc. Sci. Fenn. 19, 1–170 (1892).
    Google Scholar 
    86.Chikovani, N. & Svanidze, T. Checklist of bryophyte species of Georgia. Braun-Blanquetia 34, 97–116. https://doi.org/10.13158/heia.26.1.2013.213 (2004).Article 

    Google Scholar 
    87.Doroshina, G. Y. New moss records from Georgia. 1. Arctoa 19, 281 (2010).
    Google Scholar 
    88.Sohrabi, M., Ahti, T. & Urbanavichus, G. Parmelioid lichens of Iran and the caucasus Region. Mycol. Balc. 4, 21–30 (2007).
    Google Scholar 
    89.Hawksworth, D. L., Blanco, O., Divakar, P. K., Ahti, T. & Crespo, A. A first checklist of parmelioid and similar lichens in Europe and some adjacent territories, adopting revised generic circumscriptions and with indications of species distributions. Lichenologist 40(1), 1–21. https://doi.org/10.1017/S0024282908007329 (2008).Article 

    Google Scholar 
    90.Syrek, M. & Kukwa, M. Taxonomy of the lichen Cladonia rei and its status in Poland. Biologia 63(4), 493–497. https://doi.org/10.2478/s11756-008-0092-1 (2008).Article 

    Google Scholar 
    91.Burgaz, A. R., Ahti, T., Inashvili, T., Batsatsashvili, K. & Kupradze, I. Study of georgian Cladoniaceae. Bot. Complut. 42, 19–55. https://doi.org/10.5209/BOCM.61367 (2018).Article 

    Google Scholar 
    92.Fałtynowicz, W. The lichens, lichenicolous and allied fungi of Poland. An annotated checklist. In Biodiversity of Poland (ed. Mirek, A.) 1–435 (W. Szafer Institute of Botany, Polish Academy of Sciences, 2003).
    Google Scholar 
    93.Plášek, V., Sawicki, J., Ochyra, R., Szczecińska, M. & Kulik, T. New taxonomical arrangement of the traditionally conceived genera Orthotrichum and Ulota (Orthotrichaceae, Bryophyta). Acta Mus. Sil. 64, 169–174. https://doi.org/10.1515/cszma-2015-0024 (2015).Article 

    Google Scholar 
    94.Lara, F. et al. Lewinskya, a new genus to accommodate the phaneroporous and monoicous taxa of Orthotrichum (Bryophyta, Orthotrichaceae). Cryptog. Bryol. 37, 361–382. https://doi.org/10.7872/cryb/v37.iss4.2016.361 (2016).Article 

    Google Scholar 
    95.Sawicki, J. et al. Mitogenomic analyses support the recent division of the genus Orthotrichum (Orthotrichaceae, Bryophyta). Sci. Rep. 7, 4408. https://doi.org/10.1038/s41598-017-04833-z (2017).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    96.Kürschner, H., Batsatsashvili, K. & Parolly, G. Noteworthy additions to the bryophyte flora of Georgia. Herzogia 26, 213–216. https://doi.org/10.13158/heia.26.1.2013.213 (2013).Article 

    Google Scholar 
    97.Ellis, L. T. et al. New national and regional bryophyte records, 49. J. Bryol. 38(4), 327–347 (2016).Article 

    Google Scholar 
    98.Ellis, L. T. et al. New national and regional bryophyte records, 51. J. Bryol. 39(2), 177–190 (2017).Article 

    Google Scholar 
    99.Eckstein, J., Garilleti, R. & Lara, F. Lewinskya transcaucasica (Orthotrichaceae, Bryopsida) sp. nov. A contribution to the bryophyte flora of Georgia. J. Bryol. 40(1), 31–38. https://doi.org/10.1080/03736687.2017.1365218 (2018).Article 

    Google Scholar 
    100.Eckstein, J. & Zündorf, H.-J. Orthotrichaceous mosses (Orthotricheae, Orthotrichaceae) of the Genera Lewinskya, Nyholmiella, Orthotrichum, Pulvigera and Ulota Contributions to the bryophyte flora of Georgia 1. Cryptog. Bryol. 38(4), 365–382. https://doi.org/10.7872/cryb/v38.iss4.2017.365 (2017).Article 

    Google Scholar 
    101.Schäfer-Verwimp, A. Orthotrichum Hedw. In Die Moose Baden-Württembergs. Band 2: Spezieller Teil (Bryophytina II, Schistostegales bis Hypnobryales) (eds Nebel, M. & Philippi, G.) 170–197 (Eugen Ulmer, 2001).
    Google Scholar 
    102.Lara, F. & Garilleti, R. Orthotrichum Hedw. In Flora briofítica Ibérica (eds Guerra, J. & Brugués, C. M.) 50–135 (Universidad de Murcia Sociedad Española de Briología, 2014).
    Google Scholar 
    103.Lewinsky, J. The genus Orthotrichum Hedw. (Orthotrichaceae, Musci) in Southeast Asia. A taxonomic revision. J. Hattori Bot. Lab. 72, 1–88 (1992).
    Google Scholar 
    104.Schäfer-Verwimp, A. & Gruber, J. P. Orthotrichum (Orthotrichaceae, Bryopsida) in Pakistan. Trop. Bryol. 21, 1–9. https://doi.org/10.11646/bde.21.1.2 (2002).Article 

    Google Scholar 
    105.Draper, I., Mazimpaka, V., Albertos, B., Garilleti, R. & Lara, F. A survey of the epiphytic bryophyte flora of the Rif and Tazzeka Mountains (northern Morocco). J. Bryol. 27, 23–34. https://doi.org/10.1179/174328205X40554 (2005).Article 

    Google Scholar 
    106.Brassard, G. R. Orthotrichum stramineum new to North America. Bryologist 87, 168 (1984).Article 

    Google Scholar 
    107.Lewinsky-Haapasaari, J. & Long, D. G. Orthotrichum stramineum Hornsch. new to China. J. Bryol. 19, 350–352. https://doi.org/10.1179/jbr.1996.19.2.350 (1996).Article 

    Google Scholar 
    108.Plášek, V. et al. A synopsis of Orthotrichum s. lato (Bryophyta, Orthotrichaceae) in China, with distribution maps and a key to determination. Plants 10, 499. https://doi.org/10.3390/plants10030499 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar  More