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    Variation in the susceptibility of urban Aedes mosquitoes infected with a densovirus

    1.
    Weaver, S. C., Charlier, C., Vasilakis, N. & Lecuit, M. Zika, chikungunya, and other emerging vector-borne viral diseases. Annu. Rev. Med. 69, 395–408 (2018).
    Article  CAS  Google Scholar 
    2.
    Kilpatrick, A. M. & Randolph, S. E. Drivers, dynamics, and control of emerging vector-borne zoonotic diseases. Lancet 380, 1946–1955 (2012).
    PubMed Central  Article  PubMed  Google Scholar 

    3.
    Koureas, M., Tsakalof, A., Tsatsakis, A. & Hadjichristodoulou, C. Systematic review of biomonitoring studies to determine the association between exposure to organophosphorus and pyrethroid insecticides and human health outcomes. Toxicol. Lett. 210, 155–168 (2012).
    Article  CAS  Google Scholar 

    4.
    Peterson Robert, K. D., Macedo Paula, A. & Davis Ryan, S. A human-health risk assessment for West Nile Virus and insecticides used in mosquito management. Environ. Health Perspect. 114, 366–372 (2006).
    Article  CAS  Google Scholar 

    5.
    Han, W., Tian, Y. & Shen, X. Human exposure to neonicotinoid insecticides and the evaluation of their potential toxicity: an overview. Chemosphere 192, 59–65 (2018).
    ADS  Article  CAS  Google Scholar 

    6.
    Hernández, A. F. et al. Toxic effects of pesticide mixtures at a molecular level: their relevance to human health. Toxicology 307, 136–145 (2013).
    Article  CAS  Google Scholar 

    7.
    Sanchez-Bayo, F. P. Insecticides mode of action in relation to their toxicity to non-target organisms. J. Environ. Anal. Toxicol. s4, 002 (2012).
    Google Scholar 

    8.
    Rivero, A., Vézilier, J., Weill, M., Read, A. F. & Gandon, S. Insecticide control of vector-borne diseases: when is insecticide resistance a problem?. PLoS Pathog. 6, e1001000 (2010).
    PubMed Central  Article  CAS  PubMed  Google Scholar 

    9.
    Hemingway, J., Hawkes, N. J., McCarroll, L. & Ranson, H. The molecular basis of insecticide resistance in mosquitoes. Insect Biochem. Mol. Biol. 34, 653–665 (2004).
    Article  CAS  Google Scholar 

    10.
    Liu, N., Xu, Q., Zhu, F. & Zhang, L. Pyrethroid resistance in mosquitoes. Insect Sci. 13, 159–166 (2006).
    Article  CAS  Google Scholar 

    11.
    Dusfour, I. et al. Management of insecticide resistance in the major Aedes vectors of arboviruses: advances and challenges. PLoS Negl. Trop. Dis. 13, e0007615 (2019).
    PubMed Central  Article  CAS  PubMed  Google Scholar 

    12.
    Faraji, A. & Unlu, I. The eye of the tiger, the thrill of the fight: effective larval and adult control measures against the Asian tiger mosquito, Aedesalbopictus (Diptera: Culicidae), in North America. J. Med. Entomol. 53, 1029–1047 (2016).
    Article  Google Scholar 

    13.
    Chan, K. L., Ho, B. C. & Chan, Y. C. Aedesaegypti (L.) and Aedesalbopictus (Skuse) in Singapore City. Bull. World Health Organ. 44, 629–633 (1971).
    PubMed Central  CAS  PubMed  Google Scholar 

    14.
    Sansinenea, E. Bacillusthuringiensis Biotechnology (Springer, New York, 2012).
    Google Scholar 

    15.
    Mulla, M. S., Darwazeh, H. A. & Zgomba, M. Effect of some environmental factors on the efficacy of Bacillussphaericus 2362 and Bacillusthuringiensis (H-14) against mosquitoes. Bull. Soc. Vector Ecol. 15, 166–175 (1990).
    Google Scholar 

    16.
    Marina, C. F., Arredondo-Jiménez, J. I., Castillo, A. & Williams, T. Sublethal effects of iridovirus disease in a mosquito. Oecologia 119, 383–388 (1999).
    ADS  Article  Google Scholar 

    17.
    Delhon, G. et al. Genome of invertebrate iridescent virus type 3 (mosquito iridescent virus). J. Virol. 80, 8439–8449 (2006).
    PubMed Central  Article  CAS  PubMed  Google Scholar 

    18.
    Linley, J. R. & Nielsen, H. T. Transmission of a mosquito iridescent virus in Aedestaeniorhynchus: I. Laboratory experiments. J. Invertebr. Pathol. 12, 7–16 (1968).
    Article  CAS  Google Scholar 

    19.
    Carlson, J., Suchman, E. & Buchatsky, L. Densoviruses for control and genetic manipulation of mosquitoes. In Advances in Virus Research, Vol. 68 361–392 (Academic Press, 2006).

    20.
    Johnson, R. M. & Rasgon, J. L. Densonucleosis viruses (‘densoviruses’) for mosquito and pathogen control. Curr. Opin. Insect Sci. 28, 90–97 (2018).
    Article  Google Scholar 

    21.
    Grenet, A.-S.G. et al. Les densovirus: une «massive attaque» chez les arthropodes. Virologie 19, 19–31 (2015).
    Google Scholar 

    22.
    Hewson, I. et al. Densovirus associated with sea-star wasting disease and mass mortality. Proc. Natl. Acad. Sci. 111, 17278–17283 (2014).
    ADS  Article  CAS  Google Scholar 

    23.
    Afanasiev, B. N., Galyov, E. E., Buchatsky, L. P. & Kozlov, Y. V. Nucleotide sequence and genornic organization of aedes densonucleosis virus. Virology 185, 323–336 (1991).
    Article  CAS  Google Scholar 

    24.
    Sivaram, A. et al. Isolation and characterization of densonucleosis virus from Aedes aegypti mosquitoes and its distribution in India. Intervirology 52, 1–7 (2009).
    Article  CAS  Google Scholar 

    25.
    Chen, S. et al. Genetic, biochemical, and structural characterization of a new densovirus isolated from a chronically infected Aedesalbopictus C6/36 cell line. Virology 318, 123–133 (2004).
    Article  CAS  Google Scholar 

    26.
    Zhai, Y.-G. et al. Isolation and characterization of the full coding sequence of a novel densovirus from the mosquito Culexpipienspallens. J. Gen. Virol. 89, 195–199 (2008).
    Article  CAS  Google Scholar 

    27.
    Ren, X., Hoiczyk, E. & Rasgon, J. L. Viral Paratransgenesis in the malaria vector Anophelesgambiae. PLoS Pathog. 4, e1000135 (2008).
    PubMed Central  Article  CAS  PubMed  Google Scholar 

    28.
    Jousset, F.-X., Barreau, C., Boublik, Y. & Cornet, M. A Parvo-like virus persistently infecting a C6/36 clone of Aedesalbopictus mosquito cell line and pathogenic for Aedesaegypti larvae. Virus Res. 29, 99–114 (1993).
    Article  CAS  Google Scholar 

    29.
    Afanasiev, B. N. & Carlson, J. O. A new mosquito densovirus from Peru: genomic sequence and in vitro growth characteristics of wild type and hybrid viruses. (2003).

    30.
    O’Neill, S. L. et al. Insect densoviruses may be widespread in mosquito cell lines. J. Gen. Virol. 76, 2067–2074 (1995).
    Article  Google Scholar 

    31.
    Jousset, F.-X., Baquerizo, E. & Bergoin, M. A new densovirus isolated from the mosquito Culexpipiens (Diptera: Culicidae). Virus Res. 67, 11–16 (2000).
    Article  CAS  Google Scholar 

    32.
    Sangdee, K. & Pattanakitsakul, S. New genetic variation of Aedesalbopictus Densovirus isolated from mosquito C6/36 cell line. Southeast Asian J. Trop. Med. Public Health 43, 12 (2012).
    Google Scholar 

    33.
    Li, J. et al. A novel densovirus isolated from the asian tiger mosquito displays varied pathogenicity depending on its host species. Front. Microbiol. 10, 1549 (2019).
    PubMed Central  Article  PubMed  Google Scholar 

    34.
    Kittayapong, P., Baisley, K. J. & O’Neill, S. L. A mosquito densovirus infecting Aedesaegypti and Aedesalbopictus from Thailand. Am. J. Trop. Med. Hyg. 61, 612–617 (1999).
    Article  CAS  Google Scholar 

    35.
    Barreau, C., Jousset, F. X. & Bergoin, M. Venereal and vertical transmission of the Aedesalbopictus parvovirus in Aedesaegypti mosquitoes. Am. J. Trop. Med. Hyg. 57, 126–131 (1997).
    Article  CAS  Google Scholar 

    36.
    De Valdez, M. R. W., Suchman, E. L., Carlson, J. O. & Black, W. C. A Large Scale Laboratory Cage Trial of Aedes Densonucleosis Virus (AeDNV). J. Med. Entomol. 47, 392–399 (2010).
    Article  Google Scholar 

    37.
    Altinli, M. et al. Sharing cells with Wolbachia: the transovarian vertical transmission of Culexpipiens densovirus. Environ. Microbiol. 21, 3284–3298 (2019).
    Article  CAS  Google Scholar 

    38.
    Wei, W. et al. The pathogenicity of mosquito densovirus (C6/36DNV) and its interaction with dengue virus type II in Aedesalbopictus. Am. J. Trop. Med. Hyg. 75, 1118–1126 (2006).
    Article  Google Scholar 

    39.
    Bouyer, J., Chandre, F., Gilles, J. & Baldet, T. Alternative vector control methods to manage the Zika virus outbreak: more haste, less speed. Lancet Glob. Health 4, e364 (2016).
    Article  Google Scholar 

    40.
    Barreau, C., Jousset, F.-X. & Bergoin, M. Pathogenicity of the Aedesalbopictus parvovirus (AaPV), a denso-like virus, for Aedes aegypti mosquitoes. J. Invertebr. Pathol. 68, 299–309 (1996).
    Article  CAS  Google Scholar 

    41.
    Barreau, C., Jousset, F.-X. & Cornet, M. An efficient and easy method of infection of mosquito larvae from virus-contaminated cell cultures. J. Virol. Methods 49, 153–156 (1994).
    Article  CAS  Google Scholar 

    42.
    Igarashi, A. Isolation of a Singh’s Aedesalbopictus cell clone sensitive to dengue and chikungunya viruses. J. Gen. Virol. 40, 531–544 (1978).
    Article  CAS  Google Scholar 

    43.
    Brackney, D. E. et al. C6/36 Aedesalbopictus cells have a dysfunctional antiviral RNA interference response. PLoS Negl. Trop. Dis. 4, e856 (2010).
    PubMed Central  Article  CAS  PubMed  Google Scholar 

    44.
    Ostfeld, R. S. & Keesing, F. Effects of host diversity on infectious disease. Annu. Rev. Ecol. Evol. Syst. 43, 157–182 (2012).
    Article  Google Scholar 

    45.
    Lambrechts, L., Scott, T. W. & Gubler, D. J. Consequences of the expanding global distribution of aedes albopictus for dengue virus transmission. PLoS Negl. Trop. Dis. 4, e646 (2010).
    PubMed Central  Article  PubMed  Google Scholar 

    46.
    Ledermann, J. P., Suchman, E. L., Black, W. C. & Carlson, J. O. Infection and pathogenicity of the mosquito densoviruses AeDNV, HeDNV, and APeDNV in Aedesaegypti mosquitoes (Diptera: Culicidae). J. Econ. Entomol. 97, 1828–1835 (2004).
    Article  Google Scholar 

    47.
    Hirunkanokpun, S., Carlson, J. O. & Kittayapong, P. Evaluation of mosquito densoviruses for controlling Aedesaegypti (Diptera: Culicidae): variation in efficiency due to virus strain and geographic origin of mosquitoes. Am. J. Trop. Med. Hyg. 78, 784–790 (2008).
    Article  CAS  Google Scholar 

    48.
    Ogoyi, D. O. et al. Linkage and mapping analysis of a non-susceptibility gene to densovirus (nsd-2) in the silkworm, Bombyxmori. Insect Mol. Biol. 12, 117–124 (2003).
    Article  CAS  Google Scholar 

    49.
    Watanabe, H. & Maeda, S. Genetically determined nonsusceptibility of the silkworm, Bombyxmori, to infection with a densonucleosis virus (Densovirus). J. Invertebr. Pathol. 38, 370–373 (1981).
    Article  Google Scholar 

    50.
    Rudolf, V. H. W. & Antonovics, J. Disease transmission by cannibalism: rare event or common occurrence?. Proc. R. Soc. B Biol. Sci. 274, 1205–1210 (2007).
    Article  Google Scholar 

    51.
    Parry, R., Bishop, C., De Hayr, L. & Asgari, S. Density-dependent enhanced replication of a densovirus in Wolbachia-infected Aedes cells is associated with production of piRNAs and higher virus-derived siRNAs. Virology 528, 89–100 (2019).
    Article  CAS  Google Scholar 

    52.
    Rwegoshora, R. T., Baisley, K. J. & Kittayapong, P. Seasonal and spatial variation in natural densovirus infection in Anophelesminimus s.l. in Thailand. Southeast Asian J. Trop. Med. Public Health 31, 7 (2000).
    Google Scholar 

    53.
    Clements, A. N. The biology of mosquitoes: sensory reception and behaviour. Behaviour and aspects of the biology of larvae (1999).

    54.
    Hajek, A. E. & Shapiro-Ilan, D. I. Ecology of Invertebrate Diseases (Wiley, New York, 2018).
    Google Scholar 

    55.
    Ren, X. & Rasgon, J. L. Potential for the Anophelesgambiae densonucleosis virus to act as an “evolution-proof” biopesticide. J. Virol. 84, 7726–7729 (2010).
    PubMed Central  Article  CAS  PubMed  Google Scholar 

    56.
    Buchatsky, L. P. Densonucleosis of blood sucking mosquitoes. Dis. Aquat. Organ. 6, 145–150 (1989).
    Article  Google Scholar 

    57.
    Brengues, C. et al. Pyrethroid and DDT cross-resistance in Aedesaegypti is correlated with novel mutations in the voltage-gated sodium channel gene. Med. Vet. Entomol. 17, 87–94 (2003).
    Article  CAS  Google Scholar 

    58.
    Boublik, Y., Jousset, F.-X. & Bergoin, M. Complete nucleotide sequence and genomic organization of the Aedesalbopictus parvovirus (AaPV) pathogenic for Aedesaegypti larvae. Virology 200, 752–763 (1994).
    Article  CAS  Google Scholar  More

  • in

    High prevalence of mcr-1-encoded colistin resistance in commensal Escherichia coli from broiler chicken in Bangladesh

    1.
    Tenaillon, O., Skurnik, D., Picard, B. & Denamur, E. The population genetics of commensal Escherichia coli. Nat. Rev. Microbiol. 8, 207–217 (2010).
    CAS  PubMed  Article  Google Scholar 
    2.
    Herrero-Fresno, A., Larsen, I. & Olsen, J. E. Genetic relatedness of commensal Escherichia coli from nursery pigs in intensive pig production in Denmark and molecular characterization of genetically different strains. J. Appl. Microbiol. 119, 342–353 (2015).
    CAS  PubMed  Article  Google Scholar 

    3.
    Ahmed, S., Olsen, J. E. & Herrero-Fresno, A. The genetic diversity of commensal Escherichia coli strains isolated from nonantimicrobial treated pigs varies according to age group. PLoS ONE 12, e0178623 (2017).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    4.
    Magiorakos, A.-P. et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin. Microbiol. Infect. 18, 268–281 (2012).
    CAS  PubMed  Article  Google Scholar 

    5.
    de Been, M. et al. Dissemination of cephalosporin resistance genes between Escherichia coli strains from farm animals and humans by specific plasmid lineages. PLoS Genet. 10, e1004776 (2014).
    PubMed  PubMed Central  Article  Google Scholar 

    6.
    Salinas, L. et al. Diverse commensal Escherichia coli clones and plasmids disseminate antimicrobial resistance genes in domestic animals and children in a semirural community in Ecuador. mSphere 4, e00316-19 (2019).
    PubMed  PubMed Central  Article  Google Scholar 

    7.
    Marshall, B. M. & Levy, S. B. Food animals and antimicrobials: impacts on human health. Clin. Microbiol. Rev. 24, 718–733 (2011).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    8.
    Hoelzer, K. et al. Antimicrobial drug use in food-producing animals and associated human health risks: what, and how strong, is the evidence?. BMC Vet. Res. 13, 211 (2017).
    PubMed  PubMed Central  Article  Google Scholar 

    9.
    Islam, K. B. M. S., Shiraj-Um-Mahmuda, S. & Md, H.-B.-K. Antibiotic usage patterns in selected broiler farms of Bangladesh and their public health implications. J. Public Heal. Dev. Ctries. 2, 276–284 (2016).
    Google Scholar 

    10.
    Mendelson, M. et al. The One Health stewardship of colistin as an antibiotic of last resort for human health in South Africa. Lancet Infect. Dis. 18, e288–e294 (2018).
    PubMed  Article  Google Scholar 

    11.
    Xavier, B. B. et al. Identification of a novel plasmid-mediated colistin-resistance gene, mcr-2, in Escherichia coli, Belgium, June 2016. Eurosurveillance 21, 30280 (2016).
    Article  Google Scholar 

    12.
    Yin, W. et al. Novel plasmid-mediated colistin resistance gene mcr-3 in Escherichia coli. MBio 8, e00543-17 (2017).
    PubMed  PubMed Central  Article  Google Scholar 

    13.
    Carattoli, A. et al. Novel plasmid-mediated colistin resistance mcr-4 gene in Salmonella and Escherichia coli, Italy 2013, Spain and Belgium, 2015 to 2016. Euro Surveill. 22, 30589 (2017).
    PubMed  PubMed Central  Article  Google Scholar 

    14.
    Borowiak, M. et al. Identification of a novel transposon-associated phosphoethanolamine transferase gene, mcr-5, conferring colistin resistance in d-tartrate fermenting Salmonella enterica subsp enterica serovar Paratyphi B. J. Antimicrob. Chemother. 72, 3317–3324 (2017).
    CAS  PubMed  Article  Google Scholar 

    15.
    AbuOun, M. et al. mcr-1 and mcr-2 variant genes identified in Moraxella species isolated from pigs in Great Britain from 2014 to 2015. J. Antimicrob. Chemother. 72, 2745–2749 (2017).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    16.
    Yang, Y.-Q., Li, Y.-X., Lei, C.-W., Zhang, A.-Y. & Wang, H.-N. Novel plasmid-mediated colistin resistance gene mcr-7.1 in Klebsiella pneumoniae. J. Antimicrob. Chemother. 73, 1791–1795 (2018).
    CAS  PubMed  Article  Google Scholar 

    17.
    Wang, X. et al. Emergence of a novel mobile colistin resistance gene, mcr-8 NDM-producing Klebsiella pneumoniae. Emerg. Microbes Infect. 7, 1–9 (2018).
    PubMed Central  PubMed  Google Scholar 

    18.
    Carroll, L. M. et al. Identification of novel mobilized colistin resistance gene mcr-9 in a multidrug-resistant, colistin-susceptible Salmonella enterica serotype Typhimurium isolate. MBio 10, e00853-e919 (2019).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    19.
    Liu, Y.-Y. et al. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect. Dis. 16, 161–168 (2016).
    PubMed  Article  CAS  Google Scholar 

    20.
    Ahmed, S., Olsen, J. E. & Herrero-Fresno, A. The genetic diversity of commensal Escherichia coli strains isolated from non-antimicrobial treated pigs varies according to age group. PLoS ONE 12, e0178623 (2017).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    21.
    Katouli, M. et al. Phenotypic characterization of intestinal Escherichia coli of pigs during suckling, postweaning, and fattening periods. Appl. Environ. Microbiol. 61, 778–783 (1995).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    22.
    Bok, E., Mazurek, J. & Stosik, M. P. Age as a factor influencing diversity of commensal E. coli microflora in pigs. Polish J. Microbiol. 62, 165–171 (2013).
    Article  Google Scholar 

    23.
    Eiamphungporn, W. et al. Prevalence of the colistin resistance gene mcr-1 in colistin-resistant Escherichia coli and Klebsiella pneumoniae isolated from humans in Thailand. J. Glob. Antimicrob. Resist. 15, 32–35 (2018).
    PubMed  Article  Google Scholar 

    24.
    Li, X. et al. The prevalence of mcr-1 and resistance characteristics of Escherichia coli isolates from diseased and healthy pigs. Diagn. Microbiol. Infect. Dis. 91, 63–65 (2018).
    CAS  PubMed  Article  Google Scholar 

    25.
    Irrgang, A. et al. Prevalence of mcr-1 in E. coli from livestock and food in Germany, 2010–2015. PLoS ONE 11, e0159863 (2016).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    26.
    Quan, J. et al. Prevalence of mcr-1 in Escherichia coli and Klebsiella pneumoniae recovered from bloodstream infections in China: a multicentre longitudinal study. Lancet Infect. Dis. 17, 400–410 (2017).
    CAS  PubMed  Article  Google Scholar 

    27.
    Cao, L., Li, X., Xu, Y. & Shen, J. Prevalence and molecular characteristics of mcr-1 colistin resistance in Escherichia coli: isolates of clinical infection from a Chinese University Hospital. Infect. Drug Resist. 11, 1597–1603 (2018).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    28.
    Yi, L., Liu, Y., Wu, R., Liang, Z. & Liu, J.-H. Research progress on the plasmid-mediated colistin resistance gene mcr-1. Yi chuan 39, 110–126 (2017).
    PubMed  Google Scholar 

    29.
    Amin, M. B. et al. Occurrence and genetic characteristics of mcr-1-positive colistin-resistant E. coli from poultry environments in Bangladesh. J. Glob. Antimicrob. Resist. 22, 546–552 (2020).
    PubMed  Article  Google Scholar 

    30.
    Zając, M. et al. Occurrence and characterization of mcr-1-positive Escherichia coli isolated from food-producing animals in Poland, 2011–2016. Front. Microbiol. 10, 1753 (2019).
    PubMed  PubMed Central  Article  Google Scholar 

    31.
    Maciuca, I. E. et al. Genetic features of mcr-1 mediated colistin resistance in CMY-2-producing Escherichia coli from Romanian poultry. Front. Microbiol. 10, 2267 (2019).
    PubMed  PubMed Central  Article  Google Scholar 

    32.
    Zhang, P. et al. Characterization of five Escherichia coli isolates co-expressing ESBL and mcr-1 resistance mechanisms from different origins in China. Front. Microbiol. 10, 1994 (2019).
    PubMed  PubMed Central  Article  Google Scholar 

    33.
    Bengtsson-Palme, J., Kristiansson, E. & Larsson, D. G. J. Environmental factors influencing the development and spread of antibiotic resistance. FEMS Microbiol. Rev. 42, 68–80 (2018).
    CAS  Article  Google Scholar 

    34.
    Poulsen, L. L. et al. Longitudinal study of transmission of Escherichia coli from broiler breeders to broilers. Vet. Microbiol. 207, 13–18 (2017).
    PubMed  Article  PubMed Central  Google Scholar 

    35.
    Nilsson, O., Börjesson, S., Landén, A. & Bengtsson, B. Vertical transmission of Escherichia coli carrying plasmid-mediated AmpC (pAmpC) through the broiler production pyramid. J. Antimicrob. Chemother. 69, 1497–1500 (2014).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    36.
    Lukjancenko, O., Wassenaar, T. M. & Ussery, D. W. Comparison of 61 sequenced Escherichia coli genomes. Microb. Ecol. 60, 708–720 (2010).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    37.
    Fukiya, S., Mizoguchi, H., Tobe, T. & Mori, H. Extensive genomic diversity in pathogenic Escherichia coli and Shigella strains revealed by comparative genomic hybridization microarray. J. Bacteriol. 186, 3911–3921 (2004).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    38.
    Touchon, M. et al. Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet. 5, e1000344 (2009).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    39.
    Tettelin, H. et al. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: Implications for the microbial ‘pan-genome’. Proc. Natl. Acad. Sci. 102, 13950–13955 (2005).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    40.
    Yamamoto, T. & Echeverria, P. Detection of the enteroaggregative Escherichia coli heat-stable enterotoxin 1 gene sequences in enterotoxigenic E. coli strains pathogenic for humans. Infect. Immun. 64, 1441–1445 (1996).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    41.
    Levine, M. M. Escherichia coli that cause diarrhea: enterotoxigenic, enteropathogenic, enteroinvasive, enterohemorrhagic, and enteroadherent. J. Infect. Dis. 155, 377–389 (1987).
    CAS  PubMed  Article  Google Scholar 

    42.
    Johnson, T. J., Wannemuehler, Y. M. & Nolan, L. K. Evolution of the iss gene in Escherichia coli. Appl. Environ. Microbiol. 74, 2360–2369 (2008).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    43.
    Kocsis, E., Lo Cascio, G., Piccoli, M., Cornaglia, G. & Mazzariol, A. KPC-3 carbapenemase harbored in FIIk plasmid from Klebsiella pneumoniae ST512 and Escherichia coli ST43 in the same patient. Microb. Drug Resist. 20, 377–382 (2014).
    CAS  PubMed  Article  Google Scholar 

    44.
    Chiluisa-Guacho, C. et al. First detection of the CTXM-15 producing Escherichia coli O25-ST131 pandemic clone in Ecuador. Pathogens 7, 42 (2018).
    PubMed Central  Article  CAS  PubMed  Google Scholar 

    45.
    Karami, N., Nowrouzian, F., Adlerberth, I. & Wold, A. E. Tetracycline resistance in Escherichia coli and persistence in the infantile colonic microbiota. Antimicrob. Agents Chemother. 50, 156–161 (2006).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    46.
    Monira, S. et al. Multi-drug resistant pathogenic bacteria in the gut of young children in Bangladesh. Gut Pathog. 9, 19 (2017).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    47.
    Bryan, A., Shapir, N. & Sadowsky, M. J. Frequency and distribution of tetracycline resistance genes in genetically diverse, nonselected, and nonclinical Escherichia coli strains isolated from diverse human and animal sources. Appl. Environ. Microbiol. 70, 2503–2507 (2004).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    48.
    Birgy, A. et al. CTX-M-55-, MCR-1-, and FosA-producing multidrug-resistant Escherichia coli infection in a child in France. Antimicrob. Agents Chemother. 62, e00127-e218 (2018).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    49.
    Nakamura, S., Nakamura, M., Kojima, T. & Yoshida, H. gyrA and gyrB mutations in quinolone-resistant strains of Escherichia coli. Antimicrob. Agents Chemother. 33, 254–255 (1989).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    50.
    Vila, J., Ruiz, J., Goñi, P. & De Anta, M. T. Detection of mutations in parC in quinolone-resistant clinical isolates of Escherichia coli. Antimicrob. Agents Chemother. 40, 491–493 (1996).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    51.
    Heisig, P., Schedletzky, H. & Falkenstein-Paul, H. Mutations in the gyrA gene of a highly fluoroquinolone-resistant clinical isolate of Escherichia coli. Antimicrob. Agents Chemother. 37, 696–701 (1993).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    52.
    Esperón, F. et al. Detection of plasmid-mediated colistin resistance (mcr-1) in E. coli isolated from pig caecum in Austria. Abstr. Int. J. Infect. Dis. 53, 4–163 (2016).
    Google Scholar 

    53.
    Matamoros, S. et al. Global phylogenetic analysis of Escherichia coli and plasmids carrying the mcr-1 gene indicates bacterial diversity but plasmid restriction. Sci. Rep. 7, 15364 (2017).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    54.
    Zurfluh, K., Klumpp, J., Nüesch-Inderbinen, M. & Stephan, R. Full-length nucleotide sequences of mcr-1-harboring plasmids isolated from extended-spectrum-β-lactamase-producing Escherichia coli isolates of different origins. Antimicrob. Agents Chemother. 60, 5589–5591 (2016).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    55.
    Snesrud, E. et al. A Model for transposition of the colistin resistance gene mcr-1 by ISApl1. Antimicrob. Agents Chemother. 60, 6973–6976 (2016).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    56.
    Miles, A. A., Misra, S. S. & Irwin, J. O. The estimation of the bactericidal power of the blood. J. Hyg. (Lond) 38, 732–749 (1938).
    CAS  Google Scholar 

    57.
    Godambe, L. P., Bandekar, J. & Shashidhar, R. Species specific PCR based detection of Escherichia coli from Indian foods. 3 Biotech 7, 130 (2017).
    PubMed  PubMed Central  Article  Google Scholar 

    58.
    Rebelo, A. R. et al. Multiplex PCR for detection of plasmid-mediated colistin resistance determinants, mcr-1, mcr-2, mcr-3, mcr-4 and mcr-5 for surveillance purposes. Eurosurveillance 23, 17–00672 (2018).
    PubMed Central  Article  PubMed  Google Scholar 

    59.
    International Standards Organisation. Clinical laboratory testing and in vitro diagnostic test systems—Susceptibility testing of infectious agents and evaluation of performance of antimicrobial susceptibility test devices. Part 1: reference method for testing the in vitro activity of antimi. ISO 20776-1 (2006).

    60.
    Mohapatra, B. R., Broersma, K. & Mazumder, A. Comparison of five rep-PCR genomic fingerprinting methods for differentiation of fecal Escherichia coli from humans, poultry and wild birds. FEMS Microbiol. Lett. 277, 98–106 (2007).
    CAS  PubMed  Article  Google Scholar 

    61.
    Heras, J. et al. GelJ—a tool for analyzing DNA fingerprint gel images. BMC Bioinformatics 16, 270 (2015).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    62.
    Shannon, C. E. A mathematical theory of communication. Bell Syst. Tech. J. 27, 379–423 (1948).
    MathSciNet  MATH  Article  Google Scholar 

    63.
    Andrews S. No TitleFastQC: A Quality Control Tool for High Throughput Sequence Data. Available online at: https://www.bioinformatics.babraham.ac.uk/projects/fastqc (2010).

    64.
    Afgan, E. et al. The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2016 update. Nucleic Acids Res. 44, W3–W10 (2016).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    65.
    Wick, R. R., Judd, L. M., Gorrie, C. L. & Holt, K. E. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLOS Comput. Biol. 13, e1005595 (2017).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    66.
    Gurevich, A., Saveliev, V., Vyahhi, N. & Tesler, G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 29, 1072–1075 (2013).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    67.
    Seemann, T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068–2069 (2014).
    CAS  PubMed  Article  Google Scholar 

    68.
    Page, A. J. et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 31, 3691–3693 (2015).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    69.
    Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    70.
    Hadfield, J. et al. Phandango: an interactive viewer for bacterial population genomics. Bioinformatics 34, 292–293 (2018).
    CAS  PubMed  Article  Google Scholar 

    71.
    Wang, R. et al. The global distribution and spread of the mobilized colistin resistance gene mcr-1. Nat. Commun. 9, 1179 (2018).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    72.
    Seemann T. snippy: Fast Bacterial Variant Calling from NGS Reads. https://github.com/tseemann/snippy (2015).

    73.
    Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490 (2010).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    74.
    Letunic, I. & Bork, P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 44, W242–W245 (2016).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    75.
    Zankari, E. et al. Identification of acquired antimicrobial resistance genes. J. Antimicrob. Chemother. 67, 2640–2644 (2012).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    76.
    Joensen, K. G. et al. Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic Escherichia coli. J. Clin. Microbiol. 52, 1501–1510 (2014).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    77.
    Larsen, M. V. et al. Multilocus sequence typing of total-genome-sequenced bacteria. J. Clin. Microbiol. 50, 1355–1361 (2012).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    78.
    Carattoli, A. et al. In Silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob. Agents Chemother. 58, 3895–3903 (2014).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    79.
    Joensen, K. G., Tetzschner, A. M. M., Iguchi, A., Aarestrup, F. M. & Scheutz, F. Rapid and easy in silico serotyping of Escherichia coli isolates by use of whole-genome sequencing data. J. Clin. Microbiol. 53, 2410–2426 (2015).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    80.
    Siguier, P., Perochon, J., Lestrade, L., Mahillon, J. & Chandler, M. ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res. 34, D32–D36 (2006).
    CAS  PubMed  Article  Google Scholar 

    81.
    RcoreTeam. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: https://www.r-project.org/ (2016).

    82.
    Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
    Article  Google Scholar  More

  • in

    Fine-scale tracking of wild waterfowl and their impact on highly pathogenic avian influenza outbreaks in the Republic of Korea, 2014–2015

    1.
    Webster, R. G., Bean, W. J., Gorman, O. T., Chambers, T. M. & Kawaoka, Y. Evolution and ecology of influenza A viruses. Microbiol. Rev. 56, 152–179 (1992).
    CAS  PubMed  PubMed Central  Article  Google Scholar 
    2.
    Russell, C. J., Hu, M. & Okda, F. A. Influenza hemagglutinin protein stability, activation, and pandemic risk. Trends Microbiol. 26(10), 841–853 (2018).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    3.
    Elçi, C. The impact of HPAI of the H5N1 strain on economies of affected countries. In Human and Economic Resources Proceedings Book 101 (2006).

    4.
    Jhung, M. A. & Nelson, D. I. Outbreaks of avian influenza A (H5N2), (H5N8), and (H5N1) among birds—United States, December 2014–January 2015 (2015).

    5.
    Su, S. et al. Epidemiology, evolution, and recent outbreaks of avian influenza virus in China. J. Virol. 89, 8671–8676 (2015).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    6.
    Kim, H.-R. et al. Pathologic changes in wild birds infected with highly pathogenic avian influenza A (H5N8) viruses, South Korea, 2014. Emerg. Infect. Dis. 21, 775 (2015).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    7.
    Feare, C. J. Role of wild birds in the spread of highly pathogenic avian influenza virus H5N1 and implications for global surveillance. Avian Dis. 54, 201–212 (2010).
    PubMed  Article  Google Scholar 

    8.
    Costa, T. P., Brown, J. D., Howerth, E. W. & Stallknecht, D. E. Variation in viral shedding patterns between different wild bird species infected experimentally with low-pathogenicity avian influenza viruses that originated from wild birds. Avian Pathol. 40, 119–124 (2011).
    PubMed  Article  Google Scholar 

    9.
    Bengtsson, D. et al. Does influenza A virus infection affect movement behaviour during stopover in its wild reservoir host?. R. Soc. Open Sci. 3, 150633 (2016).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    10.
    Son, K. et al. Experimental infection of highly pathogenic avian influenza viruses, clade 2.3. 4.4 H5N6 and H5N8, in mandarin ducks from South Korea. Transboundary Emerg. Dis. 65, 899–903 (2018).
    CAS  Article  Google Scholar 

    11.
    van Dijk, J. G. B., Fouchier, R. A. M., Klaassen, M. & Matson, K. D. Minor differences in body condition and immune status between avian influenza virus-infected and noninfected mallards: a sign of coevolution?. Ecol. Evol. 5, 436–449 (2015).
    PubMed  Article  Google Scholar 

    12.
    van Dijk, J. G. B. et al. Weak negative associations between avian influenza virus infection and movement behaviour in a key host species, the mallard Anas platyrhynchos. Oikos 124, 1293–1303 (2015).
    Article  Google Scholar 

    13.
    Lee, Y.-J. et al. Novel reassortant influenza A (H5N8) viruses, South Korea, 2014. Emerg. Infect. Dis. 20, 1087 (2014).
    PubMed  PubMed Central  Google Scholar 

    14.
    Lee, D.-H. et al. Intercontinental spread of Asian-origin H5N8 to North America through Beringia by migratory birds. J. Virol. 89, 6521–6524 (2015).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    15.
    Verhagen, J. J. et al. Wild bird surveillance around outbreaks of highly pathogenic avian influenza A (H5N8) virus in the Netherlands, 2014, within the context of global flyways. Eurosurveillance 20, 21–32 (2015).
    Article  Google Scholar 

    16.
    Shin, J.-H. et al. Prevalence of avian influenza virus in wild birds before and after the HPAI H5N8 outbreak in 2014 in South Korea. J. Microbiol. 53, 475–480 (2015).
    CAS  PubMed  Article  Google Scholar 

    17.
    Jeong, J. et al. Highly pathogenic avian influenza virus (H5N8) in domestic poultry and its relationship with migratory birds in South Korea during 2014. Vet. Microbiol. 173, 249–257 (2014).
    PubMed  Article  Google Scholar 

    18.
    Fourment, M., Darling, A. E. & Holmes, E. C. The impact of migratory flyways on the spread of avian influenza virus in North America. BMC Evol. Biol. 17, 118 (2017).
    PubMed  PubMed Central  Article  Google Scholar 

    19.
    Kwon, Y. et al. An outbreak of highly pathogenic avian influenza subtype H5N1 in broiler breeders, Korea. J. Vet. Med. Sci. 67, 1193–1196 (2005).
    PubMed  Article  Google Scholar 

    20.
    Lee, Y.-J. et al. Highly pathogenic avian influenza virus (H5N1) in domestic poultry and relationship with migratory birds, South Korea. Emerg. Infect. Dis. 14, 487 (2008).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    21.
    Lycett, S. J. et al. Role for migratory wild birds in the global spread of avian influenza H5N8. Science 354, 213–217 (2016).
    Article  CAS  Google Scholar 

    22.
    Lee, D.-H. et al. Pathogenicity of the Korean H5N8 highly pathogenic avian influenza virus in commercial domestic poultry species. Avian Pathol. 45, 208–211 (2016).
    CAS  PubMed  Article  Google Scholar 

    23.
    Bouwstra, R. J. et al. Phylogenetic analysis of highly pathogenic avian influenza A (H5N8) virus outbreak strains provides evidence for four separate introductions and one between-poultry farm transmission in the Netherlands, November 2014. Eurosurveillance 20, 21174 (2015).
    PubMed  Article  Google Scholar 

    24.
    Hanna, A. et al. Genetic characterization of highly pathogenic avian influenza (H5N8) virus from domestic ducks, England, November 2014. Emerg. Infect. Dis. 21, 879 (2015).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    25.
    Kanehira, K. et al. Characterization of an H5N8 influenza A virus isolated from chickens during an outbreak of severe avian influenza in Japan in April 2014. Adv. Virol. 160, 1629–1643 (2015).
    CAS  Google Scholar 

    26.
    Pohlmann, A. et al. Outbreaks among wild birds and domestic poultry caused by reassorted influenza A (H5N8) clade 2.3. 4.4 viruses, Germany, 2016. Emerg. Infect. Dis. 23, 633 (2017).
    PubMed  PubMed Central  Article  Google Scholar 

    27.
    Guinat, C. et al. Spatio-temporal patterns of highly pathogenic avian influenza virus subtype H5N8 spread, France, 2016 to 2017. Eurosurveillance 23, 1700791 (2018).
    PubMed Central  Article  PubMed  Google Scholar 

    28.
    Lee, D.-H. et al. Highly pathogenic avian influenza viruses and generation of novel reassortants, United States, 2014–2015. Emerg. Infect. Dis. 22, 1283 (2016).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    29.
    Kwon, J.-H. et al. Highly pathogenic avian influenza A (H5N8) viruses reintroduced into South Korea by migratory waterfowl, 2014–2015. Emerg. Infect. Dis. 22, 507 (2016).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    30.
    Kang, H.-M. et al. Novel reassortant influenza A (H5N8) viruses among inoculated domestic and wild ducks, South Korea, 2014. Emerg. Infect. Dis. 21, 298 (2015).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    31.
    Hoye, B. J., Munster, V. J., Nishiura, H., Klaassen, M. & Fouchier, R. A. M. Surveillance of wild birds for avian influenza virus. Emerg. Infect. Dis. 16, 1827–1834 (2010).
    PubMed  PubMed Central  Article  Google Scholar 

    32.
    Kays, R., Crofoot, M. C., Jetz, W. & Wikelski, M. Terrestrial animal tracking as an eye on life and planet. Science 348, aaa2478 (2015).
    PubMed  Article  CAS  Google Scholar 

    33.
    Hussey, N. E. et al. Aquatic animal telemetry: a panoramic window into the underwater world. Science 348, 1255642 (2015).
    PubMed  Article  CAS  Google Scholar 

    34.
    Goldingay, R. & Kavanagh, R. Home-range estimates and habitat of the yellow-bellied glider (Petaurus australis) at Waratah Creek, New South Wales. Wildl. Res. 20, 387 (1993).
    Article  Google Scholar 

    35.
    Karanth, K. U. & Nichols, J. D. Estimation of tiger densities in india using photographic captures and recaptures. Ecology 79, 2852–2862 (1998).
    Article  Google Scholar 

    36.
    Horne, J. S., Garton, E. O., Krone, S. M. & Lewis, J. S. Analyzing animal movements using Brownian bridges. Ecology 88, 2354–2363 (2007).
    PubMed  Article  Google Scholar 

    37.
    Fischer, J. W., Walter, W. D. & Avery, M. L. Brownian bridge movement models to characterize birds’ home ranges. Condor 115, 298–305 (2013).
    Article  Google Scholar 

    38.
    Kranstauber, B., Kays, R., LaPoint, S. D., Wikelski, M. & Safi, K. A dynamic Brownian bridge movement model to estimate utilization distributions for heterogeneous animal movement. J. Anim. Ecol. 81, 738–746 (2012).
    PubMed  Article  Google Scholar 

    39.
    Takekawa, J. Y. et al. Migration of waterfowl in the East Asian flyway and spatial relationship to HPAI H5N1 outbreaks. Avian Dis. 54, 466–476 (2010).
    PubMed  PubMed Central  Article  Google Scholar 

    40.
    Cappelle, J. et al. Risks of avian influenza transmission in areas of intensive free-ranging duck production with wild waterfowl. EcoHealth 11, 109–119 (2014).
    PubMed  PubMed Central  Article  Google Scholar 

    41.
    Gaidet, N. et al. Potential spread of highly pathogenic avian influenza H5N1 by wildfowl: dispersal ranges and rates determined from large-scale satellite telemetry. J. Appl. Ecol. 47, 1147–1157 (2010).
    Article  Google Scholar 

    42.
    Gilbert, M. et al. Could Changes in the agricultural landscape of northeastern China have influenced the long-distance transmission of Highly pathogenic avian influenza H5nx Viruses?. Front. Vet. Sci. 4, 225 (2017).
    PubMed  PubMed Central  Article  Google Scholar 

    43.
    Palm, E. C. et al. Mapping migratory flyways in Asia using dynamic Brownian bridge movement models. Movement Ecol. 3, 3 (2015).
    Article  Google Scholar 

    44.
    Viana, D. S., Santamaría, L. & Figuerola, J. Migratory birds as global dispersal vectors. Trends Ecol. Evol. 31, 763–775 (2016).
    PubMed  Article  Google Scholar 

    45.
    Helm, B. & Gwinner, E. Migratory restlessness in an equatorial nonmigratory bird. PLoS Biol. 4, e110 (2006).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    46.
    Velkers, F. C., Blokhuis, S. J., Veldhuis Kroeze, E. J. B. & Burt, S. A. The role of rodents in avian influenza outbreaks in poultry farms: a review. Vet. Q. 37, 182–194 (2017).
    PubMed  Article  Google Scholar 

    47.
    Lee, K. et al. Highly pathogenic avian influenza A (H5N6) in domestic cats, South Korea. Emerg. Infect. Dis. 24, 2343 (2018).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    48.
    Hill, S. C. et al. Wild waterfowl migration and domestic duck density shape the epidemiology of highly pathogenic H5N8 influenza in the Republic of Korea. Infect. Genet. Evol. 34, 267–277 (2015).
    PubMed  PubMed Central  Article  Google Scholar 

    49.
    Tiensin, T. et al. ecologic risk factor investigation of clusters of avian influenza A (H5N1) virus infection in Thailand. J. Infect. Dis. 199, 1735–1743 (2009).
    PubMed  Article  Google Scholar 

    50.
    Martin, V. et al. Spatial distribution and risk factors of highly pathogenic avian influenza (HPAI) H5N1 in China. PLoS Pathog. 7, e1001308 (2011).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    51.
    Kwon, J.-H. et al. Domestic ducks play a major role in the maintenance and spread of H5N8 highly pathogenic avian influenza viruses in South Korea. Transbound. Emerg. Dis. https://doi.org/10.1111/tbed.13406 (2019).
    Article  PubMed  Google Scholar 

    52.
    Kim, W. et al. Risk factors associated with highly pathogenic avian influenza subtype H5N8 outbreaks on broiler duck farms in South Korea. Transbound. Emerg. Dis. 65, 1329–1338 (2018).
    PubMed  Article  Google Scholar 

    53.
    Hicks, J. T. et al. Agricultural and geographic factors shaped the North American 2015 highly pathogenic avian influenza H5N2 outbreak. PLoS Pathog. 16, e1007857 (2020).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    54.
    Lu, L., Leigh Brown, A. J. & Lycett, S. J. Quantifying predictors for the spatial diffusion of avian influenza virus in China. BMC Evol. Biol. 17, 16 (2017).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    55.
    Brown, J. D., Stallknecht, D. E., Beck, J. R., Suarez, D. L. & Swayne, D. E. Susceptibility of North American ducks and gulls to H5N1 highly pathogenic avian influenza viruses. Emerg. Infect. Dis. 12, 1663–1670 (2006).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    56.
    Newman, S. H. et al. Eco-virological approach for assessing the role of wild birds in the spread of avian influenza H5N1 along the Central Asian Flyway. PLoS ONE 7, e30636 (2012).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    57.
    Wikelski, M. & Kays, R. Movebank: Archive, Analysis and Sharing of Animal Movement Data. World Wide Web electronic publication (2014).

    58.
    La Sorte, F. A., Fink, D., Hochachka, W. M. & Kelling, S. Convergence of broad-scale migration strategies in terrestrial birds. Proc. R. Soc. B Biol. Sci. 283, 20152588 (2016).
    Article  CAS  Google Scholar 

    59.
    Németh, B. et al. Comparison of weighting methods used in multicriteria decision analysis frameworks in healthcare with focus on low-and middle-income countries. J. Comp. Effect. Res. 8, 195–204 (2019).
    Article  Google Scholar 

    60.
    Belkhiria, J., Alkhamis, M. A. & Martínez-López, B. Application of Species Distribution Modeling for Avian Influenza surveillance in the United States considering the North America Migratory Flyways. Sci. Rep. 6, 33161 (2016).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    61.
    Belkhiria, J., Hijmans, R. J., Boyce, W., Crossley, B. M. & Martínez-López, B. Identification of high risk areas for avian influenza outbreaks in California using disease distribution models. PLoS ONE 13, e0190824 (2018).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    62.
    Stevens, K. B., Gilbert, M. & Pfeiffer, D. U. Modeling habitat suitability for occurrence of highly pathogenic avian influenza virus H5N1 in domestic poultry in Asia: a spatial multicriteria decision analysis approach. Spat. Spatio-temporal Epidemiol. 4, 1–14 (2013).
    Article  Google Scholar 

    63.
    Martin, V. et al. Risk-based surveillance for avian influenza control along poultry market chains in South China: the value of social network analysis. Prev. Vet. Med. 102, 196–205 (2011).
    ADS  PubMed  PubMed Central  Article  Google Scholar 

    64.
    Fournié, G. et al. Interventions for avian influenza A (H5N1) risk management in live bird market networks. PNAS 110, 9177–9182 (2013).
    ADS  PubMed  Article  Google Scholar 

    65.
    Poolkhet, C., Chairatanayuth, P., Thongratsakul, S., Kasemsuwan, S. & Rukkwamsuk, T. Social network analysis used to assess the relationship between the spread of avian influenza and movement patterns of backyard chickens in Ratchaburi, Thailand. Res. Vet. Sci. 95, 82–86 (2013).
    PubMed  Article  Google Scholar 

    66.
    Wiratsudakul, A. et al. Modeling the dynamics of backyard chicken flows in traditional trade networks in Thailand: implications for surveillance and control of avian influenza. Trop. Anim. Health Prod. 46, 845–853 (2014).
    PubMed  Article  Google Scholar 

    67.
    Lee, K. et al. Unraveling the contact patterns and network structure of pig shipments in the United States and its association with porcine reproductive and respiratory syndrome virus (PRRSV) outbreaks. Prev. Vet. Med. 138, 113–123 (2017).
    PubMed  Article  Google Scholar 

    68.
    Amirpour Haredasht, S. et al. Modeling the spatio-temporal dynamics of porcine reproductive and respiratory syndrome cases at farm level using geographical distance and pig trade network matrices. BMC Vet. Res. 13, 163 (2017).
    PubMed  PubMed Central  Article  Google Scholar 

    69.
    Kim, Y. et al. Livestock trade network: potential for disease transmission and implications for risk-based surveillance on the island of Mayotte. Sci. Rep. 8, 11550 (2018).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    70.
    McCue, M. E. & McCoy, A. M. The scope of big data in one medicine: unprecedented opportunities and challenges. Front. Vet. Sci. 4, 194 (2017).
    PubMed  PubMed Central  Article  Google Scholar 

    71.
    Boyce, W. M., Sandrock, C., Kreuder-Johnson, C., Kelly, T. & Cardona, C. Avian influenza viruses in wild birds: a moving target. Comp. Immunol. Microbiol. Infect. Dis. 32, 275–286 (2009).
    PubMed  Article  Google Scholar 

    72.
    Gardy, J. L. & Loman, N. J. Towards a genomics-informed, real-time, global pathogen surveillance system. Nat. Rev. Genet. 19, 9 (2018).
    CAS  PubMed  Article  Google Scholar 

    73.
    Hill, N. J. & Runstadler, J. A. A bird’s eye view of influenza a virus transmission: challenges with characterizing both sides of a co-evolutionary dynamic. Integr. Comp. Biol. 56, 304–316 (2016).
    PubMed  PubMed Central  Article  Google Scholar 

    74.
    Both, C., Bouwhuis, S., Lessells, C. M. & Visser, M. E. Climate change and population declines in a long-distance migratory bird. Nature 441, 81–83 (2006).
    ADS  CAS  PubMed  Article  Google Scholar 

    75.
    Rejmanek, D., Hosseini, P. R., Mazet, J. A. K., Daszak, P. & Goldstein, T. Evolutionary dynamics and global diversity of influenza A virus. J. Virol. 89, 10993–11001 (2015).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    76.
    Jenni, L. & Kéry, M. Timing of autumn bird migration under climate change: advances in long–distance migrants, delays in short–distance migrants. Proc. R. Soc. Lond. Ser. B Biol. Sci. 270, 1467–1471 (2003).
    Article  Google Scholar 

    77.
    Lee, D.-H. et al. Surveillance and Isolation of HPAI H5N1 from Wild Mandarin Ducks (Aix galericulata). J. Wildl. Dis. 47, 994–998 (2011).
    PubMed  Article  Google Scholar 

    78.
    Kim, H.-R. et al. Highly pathogenic avian influenza (H5N1) outbreaks in wild birds and poultry, South Korea. Emerg. Infect. Dis. 18, 480–483 (2012).
    PubMed  PubMed Central  Article  Google Scholar 

    79.
    Kwon, Y. K., Thomas, C. & Swayne, D. E. Variability in pathobiology of South Korean H5N1 high-pathogenicity avian influenza virus infection for 5 species of migratory waterfowl. Vet. Pathol. 47, 495–506 (2010).
    CAS  PubMed  Article  Google Scholar 

    80.
    Kranstauber, B., Smolla, M. & Kranstauber, M. B. Move: visualizing and analyzing animal track data. https://CRAN.R-project.org/package=move (2019).

    81.
    R Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (2019).

    82.
    RStudio Team. RStudio: integrated development for R. RStudio, Inc., Boston, MA https://www.rstudio.com (2019). More

  • in

    The impact of rising sea temperatures on an Arctic top predator, the narwhal

    1.
    Alexander, M. A. et al. Projected sea surface temperatures over the 21st century: changes in the mean, variability and extremes for large marine ecosystem regions of Northern Oceans. Elem. Sci. Anth. 6, 9 (2018).
    Article  Google Scholar 
    2.
    National Snow & Ice Data Center. State of the cryosphere: is the cryosphere sending signals about climate change? https://nsidc.org/cryosphere/sotc/sea_ice.html (2020). Accessed 24 Apr 2020.

    3.
    Michel, C. et al. Biodiversity of Arctic marine ecosystems and responses to climate change. Biodiversity 13, 200–214 (2012).
    Article  Google Scholar 

    4.
    Hauser, D. D. W., Laidre, K. L. & Stern, H. L. Vulnerability of Arctic marine mammals to vessel traffic in the increasingly ice-free Northwest Passage and Northern Sea Route. Proc. Natl. Acad. Sci. 115, 7617–7622 (2018).
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    5.
    Albouy, C. et al. Global vulnerability of marine mammals to global warming. Sci. Rep. 10, 1–12 (2020).
    Article  CAS  Google Scholar 

    6.
    Dietz, R., Heide-Jørgensen, M. P., Glahder, C. & Born, E. Occurrence of narwhals (Monodon monoceros) and white whales (Delphinapterus leucas) in East Greenland. Meddr. Grønl. Biosci. 39, 69–86 (1994).
    Google Scholar 

    7.
    Dietz, R., Heide-Jørgensen, M. P., Richard, P. R. & Acquarone, M. Summer and Fall Movements of Narwhals (Monodon monoceros) from Northeastern Baffin Island Towards Northern Davis Strait. Arctic 54, 244–261 (2001).
    Article  Google Scholar 

    8.
    Richard, P., Weaver, P., Dueck, L. & Barber, D. Distribution and numbers of Canadian High Arctic narwhals (Monodon monoceros) in August 1984. Meddr. Grønl. Biosci. 39, 41–50 (1994).
    Google Scholar 

    9.
    Dietz, R. & Heide-Jørgensen, M. P. Movements and swimming speed of narwhals, Monodon monoceros, equipped with satellite transmitters in Melville Bay, northwest Greenland. Can. J. Zool. 73, 2106–2119 (1995).
    Article  Google Scholar 

    10.
    Belikov, S. E. & Boltunov, A. N. Distribution and migrations of cetaceans in the Russian Arctic according to observations from aerial ice reconnaissance. NAMMCO Sci. Publ. 4, 69–86 (2002).
    Article  Google Scholar 

    11.
    Vacquié-Garcia, J. et al. Late summer distribution and abundance of ice-associated whales in the Norwegian High Arctic. Endanger. Species Res. 32, 59–70 (2017).
    Article  Google Scholar 

    12.
    Heide-Jørgensen, M., Richard, P. R., Dietz, R. & Laidre, K. L. A metapopulation model for Canadian and West Greenland narwhals. Anim. Conserv. 16, 331–343 (2013).
    Article  Google Scholar 

    13.
    Hobbs, R. C. et al. Global review of the conservation status of Monodontid stocks. Mar. Fish. Rev. 81, 1–41 (2020).
    Article  Google Scholar 

    14.
    Kovacs, K. M. & Lydersen, C. Climate change impacts on seals and whales in the North Atlantic Arctic and adjacent shelf seas. Sci. Prog. 91, 117–150 (2008).
    PubMed  Article  Google Scholar 

    15.
    Laidre, K. L. et al. Quantifying the sensitivity of Arctic marine mammals to climate-induced habitat change. Ecol. Appl. 18, S97–S125 (2008).
    PubMed  Article  Google Scholar 

    16.
    Heide-Jørgensen, M. et al. Abundance of narwhals (Monodon monoceros) on the hunting grounds in Greenland. J. Mammal. 91, 1135–1151 (2010).
    Article  Google Scholar 

    17.
    Doniol-Valcroze, T. et al. Abundance Estimates of Narwhal Stocks in the Canadian High Arctic in 2013 (NAMMCO Sci. Publ. 11, in press).

    18.
    Münchow, A., Falkner, K. K. & Melling, H. Baffin Island and West Greenland Current Systems in northern Baffin Bay. Prog. Oceanogr. 132, 305–317 (2015).
    ADS  Article  Google Scholar 

    19.
    Sutherland, D. A. & Pickart, R. S. The East Greenland coastal current: structure, variability, and forcing. Prog. Oceanogr. 78, 58–77 (2008).
    ADS  Article  Google Scholar 

    20.
    Håvik, L. et al. Structure and variability of the Shelfbreak East Greenland current North of Denmark Strait. J. Phys. Oceanogr. 47, 2631–2646 (2017).
    ADS  Article  Google Scholar 

    21.
    Heide-Jørgensen, M. P. et al. Some like it cold: temperature-dependent habitat selection by narwhals. Ecol. Evol. 10, 8073–8090 (2020).
    PubMed  PubMed Central  Article  Google Scholar 

    22.
    Heide-Jørgensen, M. P. et al. The migratory behaviour of narwhals (Monodon monoceros). Can. J. Zool. 81, 1298–1305 (2003).
    Article  Google Scholar 

    23.
    Dietz, R. et al. Movements of narwhals (Monodon monoceros) from Admiralty Inlet monitored by satellite telemetry. Polar Biol. 31, 1295–1306 (2008).
    Article  Google Scholar 

    24.
    R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (2018). Accessed 24 Apr 2019.

    25.
    Albertsen, C. M., Whoriskey, K., Yurkowski, D., Nielsen, A. & Flemming, J. M. Fast fitting of non-Gaussian state-space models to animal movement data via template model builder. Ecology 96, 2598–2604 (2015).
    PubMed  Article  PubMed Central  Google Scholar 

    26.
    Albertsen, C. M. argosTrack: Fit Movement Models to Argos Data for Marine Animals. R package version 1.2.2. https://doi.org/10.5281/zenodo.1420418, https://github.com/calbertsen/argosTrack/tree/v1.2.2 (2018). Accessed 20 Aug 2019.

    27.
    Bryant, E. 2D Location Accuracy Statistics for Fastloc® Cores Running Firmware Versions 2.2 & 2.3. (2007).

    28.
    Tomkiewicz, S. M., Fuller, M. R., Kie, J. G. & Bates, K. K. Global positioning system and associated technologies in animal behaviour and ecological research. Philos. Trans. R. Soc. B Biol. Sci. 365, 2163–2176 (2010).
    Article  Google Scholar 

    29.
    Pohlert, T. Trend: non-parametric trend tests and change-point detection. R package version, 1(0). https://cran.r-project.org/web/packages/trend/trend.pdf (2018). Accessed 10 Aug 2019.

    30.
    Heide-Jørgensen, M., Richard, P., Dietz, R. & Laidre, K. A metapopulation model for Canadian and West Greenland narwhals. Anim. Conserv. 16, 331–343 (2012).
    Article  Google Scholar 

    31.
    Komsta, L. & Komsta, M. L. Package ‘mblm’. https://cran.pau.edu.tr/web/packages/mblm/mblm.pdf (2013). Accessed 10 Aug 2019.

    32.
    Chambault, P. et al. Sea surface temperature predicts the movements of an Arctic cetacean: the bowhead whale. Sci. Rep. 8, 9658 (2018).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    33.
    Heide-Jørgensen, L. M. P. & Nielsen, T. G. Role of the bowhead whale as a predator in West Greenland. Mar. Ecol. Prog. Ser. 346, 285–297 (2008).
    Google Scholar 

    34.
    Laidre, K. L. & Heide-Jørgensen, M. P. Winter feeding intensity of narwhals (Monodon monoceros). Mar. Mammal. Sci. 21, 45–57 (2005).
    Article  Google Scholar 

    35.
    Forster, C. Spatial Patterns, Environmental Correlates, and Potential Seasonal Migration Triangle of Arctic cod (Boreogadus saida) Distribution in the Chukchi and Beaufort seas (2019).

    36.
    Laurel, B. J., Copeman, L. A., Spencer, M. & Iseri, P. Temperature-dependent growth as a function of size and age in juvenile Arctic cod (Boreogadus saida). ICES J. Mar. Sci. 74, 1614–1621 (2017).
    Article  Google Scholar 

    37.
    Laidre, K. L. et al. Seasonal narwhal habitat associations in the high Arctic. Mar. Biol. 145, 821–831 (2004).
    Google Scholar 

    38.
    Schmidt-Nielsen, K. Animal Physiology: Adaptation and Environment (Cambridge University Press, Cambridge, 1997).
    Google Scholar 

    39.
    Castellini, M. Thermoregulation. in Encyclopedia of Marine Mammals (eds Perrin, W. F. et al.) 1166–1171 (Academic Press, Cambridge, 2009).
    Google Scholar 

    40.
    Kanwisher, J. W. & Ridgway, S. H. The physiological ecology of Whales and Porpoises. Sci. Am. 248, 110–121 (1983).
    Article  Google Scholar 

    41.
    Williams, T. M., Noren, S. R. & Glenn, M. Extreme physiological adaptations as predictors of climate-change sensitivity in the narwhal Monodon monoceros. Mar. Mammal Sci. 27, 334–349 (2010).
    Article  Google Scholar 

    42.
    McLaughlin, F. A., Carmack, E. C., Ingram, R. G., Williams, W. & Michel, C. Oceanography of the Northwest Passage. in The Sea 26 (ed. Banville, J.) 1211–1242 (President and Fellows of Harvard College, Boston, 2004).
    Google Scholar 

    43.
    Kern, S., Kaleschke, L. & Spreen, G. Climatology of the Nordic (Irminger, Greenland, Barents, Kara and White/Pechora) Seas ice cover based on 85 GHz satellite microwave radiometry: 1992–2008. Tellus Dyn. Meteorol. Oceanogr. 62, 411–434 (2010).
    Article  Google Scholar 

    44.
    Hansen, R. G., Borchers, D. L. & Heide-Jørgensen, M. P. Abundance of narwhals summering in East Greenland and narwhals wintering in the North Water and Northeast Water polynyas. J. Mammal. 91, 1135–1151 (2019).
    Google Scholar 

    45.
    Riewe, R. Inuit land in the high Canadian Arctic. in Report Inuit land use and occupancy project 173–184 (1976).

    46.
    Riewe, R. The utilisation of wildlife in the Jones Sound region by Grise Fjord Inuit. in Truelove Lowland, Devon Island, Canada: A high Arctic Ecosystem 623–644 (1977).

    47.
    Riewe, R. Nunavut atlas. Canadian Circumpolar Institute and Tungavik Federation of Nunavut (1992).

    48.
    Watt, C. A., Doniol-Valcroze, T., Witting, L., Hobbs, R. C., Hansen, R. G., Lee, D. S., … & Heide-Jorgensen, M. P. (2019). Hunt allocation modeling for migrating animals: The case of Baffin Bay narwhal, Monodon monoceros. Mar. Fish. Rev, 81(3–4), 125–136.

    49.
    Witting, L., Doniol-Valcroze, T., Hobbs, R. C., Ditlevsen, S. & Heide-Jørgensen, M. Meta-population modelling of narwhals, Monodon monoceros, in East Canada and West Greenland. Mar. Fish. Rev. 81, 116–138 (2019) (in press).
    Google Scholar 

    50.
    NAMMCO. Report of the Ad hoc Working Group on Narwhal in East Greenland. https://nammco.no/wp-content/uploads/2018/05/report-global-review-of-monodontids-nammco-2018_after-erratum-060518_with-appendices_2.pdf (2019). Accessed 10 Aug 2019.

    51.
    Kvadsheim, P. H. & Folkow, L. P. Blubber and flipper heat transfer in harp seals. Acta Physiol. Scand. 161, 385–395 (1997).
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    52.
    Kvadsheim, P. H., Gotaas, A. R. L., Folkow, L. P. & Blix, A. S. An Experimental validation of heat loss models for marine mammals. J. Theor. Biol. 184, 15–23 (1997).
    Article  Google Scholar 

    53.
    Scholander, P. Evolution of climatic adaptation in homeotherms. Evolution 9, 15–26 (1955).
    Article  Google Scholar 

    54.
    Noren, D. P., Williams, T. M., Berry, P. & Butler, E. Thermoregulation during swimming and diving in bottlenose dolphins Tursiops truncatus. J. Comp. Physiol. B 169, 93–99 (1999).
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    55.
    Innes, S. et al. Surveys of belugas and narwhals in the Canadian High Arctic in 1996. NAMMCO Sci. Publ. 4, 169–190 (2002).
    Article  Google Scholar 

    56.
    Richard, P. et al. Baffin Bay Narwhal population distribution and numbers: aerial surveys in the Canadian high Arctic, 2002–04. Arctic 63, 85–99 (2010).
    Article  Google Scholar 

    57.
    Asselin, N. C. & Richard, P. Results of narwhal (Monodon monoceros) aerial surveys in Admiralty Inlet (2011).

    58.
    Hansen, R. et al. Abundance of narwhals in Melville Bay in 2012 and 2014. (2015).

    59.
    Hansen, R. & Heide-Jørgensen, M. P. Re-calculations of abundance of narwhals to three management units in East Greenland (2019). More

  • in

    Successful post-glacial colonization of Europe by single lineage of freshwater amphipod from its Pannonian Plio-Pleistocene diversification hotspot

    1.
    Hewitt, G. M. Some genetic consequences of ice ages, and their role in divergence and speciation. Biol. J. Linn. Soc. 58, 247–276. https://doi.org/10.1006/bijl.1996.0035 (1996).
    Article  Google Scholar 
    2.
    Hewitt, G. M. Genetic consequences of climatic oscillations in the quaternary. Philos. Trans. R. Soc. B Biol. Sci. 359, 183–195. https://doi.org/10.1098/rstb.2003.1388 (2004).
    CAS  Article  Google Scholar 

    3.
    Patton, H. et al. Deglaciation of the Eurasian ice sheet complex. Quat. Sci. Rev. 169, 148–172. https://doi.org/10.1016/j.quascirev.2017.05.019 (2017).
    ADS  Article  Google Scholar 

    4.
    Hewitt, G. M. Postglacial re-colonisation of European biota. Biol. J. Linn. Soc. 68, 87–112 (1999).
    Article  Google Scholar 

    5.
    Sworobowicz, L. et al. Revisiting the phylogeography of Asellus aquaticus in Europe: insights into cryptic diversity and spatiotemporal diversification. Freshw. Biol. 60, 1824–1840. https://doi.org/10.1111/fwb.12613 (2015).
    Article  Google Scholar 

    6.
    Schmitt, T. & Varga, Z. Extra-Mediterranean refugia: the rule and not the exception?. Front. Zool. 9, 1–12. https://doi.org/10.1186/1742-9994-9-22 (2012).
    Article  Google Scholar 

    7.
    Verovnik, R., Sket, B. & Trontelj, P. The colonization of Europe by the freshwater crustacean Asellus aquaticus (Crustacea: Isopoda) proceeded from ancient refugia and was directed by habitat connectivity. Mol. Ecol. 14, 4355–4369. https://doi.org/10.1111/j.1365-294X.2005.02745.x (2005).
    CAS  Article  PubMed  Google Scholar 

    8.
    Sworobowicz, L., Mamos, T., Grabowski, M. & Wysocka, A. Lasting through the ice age: the role of the proglacial refugia in the maintenance of genetic diversity, population growth, and high dispersal rate in a widespread freshwater crustacean. Freshw. Biol. https://doi.org/10.1111/fwb.13487 (2020).
    Article  Google Scholar 

    9.
    Neumann, K. et al. Genetic spatial structure of European common hamsters (Cricetus cricetus)—a result of repeated range expansion and demographic bottlenecks. Mol. Ecol. 14, 1473–1483. https://doi.org/10.1111/j.1365-294X.2005.02519.x (2005).
    CAS  Article  PubMed  Google Scholar 

    10.
    Fussi, B., Lexer, C. & Heinze, B. Phylogeography of Populus alba (L.) and Populus tremula (L.) in Central Europe: secondary contact and hybridisation during recolonisation from disconnected refugia. Tree Genet. Genomes 6, 439–450. https://doi.org/10.1007/s11295-009-0262-5 (2010).
    Article  Google Scholar 

    11.
    Grabowski, M., Mamos, T., Bącela-Spychalska, K., Rewicz, T. & Wattier, R. A. Neogene paleogeography provides context for understanding the origin and spatial distribution of cryptic diversity in a widespread Balkan freshwater amphipod. PeerJ 5, e3016. https://doi.org/10.7717/peerj.3016 (2017).
    Article  PubMed  PubMed Central  Google Scholar 

    12.
    Hou, Z., Sket, B., Fiser, C. & Li, S. Eocene habitat shift from saline to freshwater promoted Tethyan amphipod diversification. Proc. Natl. Acad. Sci. 108, 14533–14538. https://doi.org/10.1073/pnas.1104636108 (2011).
    ADS  Article  PubMed  Google Scholar 

    13.
    Mamos, T., Wattier, R., Burzyński, A. & Grabowski, M. The legacy of a vanished sea: a high level of diversification within a European freshwater amphipod species complex driven by 15 My of Paratethys regression. Mol. Ecol. 25, 795–810. https://doi.org/10.1111/mec.13499 (2016).
    Article  PubMed  Google Scholar 

    14.
    Perea, S. et al. Phylogenetic relationships and biogeographical patterns in Circum-Mediterranean subfamily Leuciscinae (Teleostei, Cyprinidae) inferred from both mitochondrial and nuclear data. BMC Evol. Biol. 10, 1–27. https://doi.org/10.1186/1471-2148-10-265 (2010).
    CAS  Article  Google Scholar 

    15.
    Saito, T. et al. Phylogeography of freshwater planorbid snails reveals diversification patterns in Eurasian continental islands. BMC Evol. Biol. https://doi.org/10.1186/s12862-018-1273-3 (2018).
    Article  PubMed  PubMed Central  Google Scholar 

    16.
    Utevsky, S. & Trontelj, P. Phylogeography of the southern medicinal leech, Hirudo verbana: a response to Živić et al. (2015). Aquat. Ecol. 50, 97–100. https://doi.org/10.1007/s10452-015-9553-0 (2016).
    CAS  Article  Google Scholar 

    17.
    Grabowski, M., Jażdżewski, K. & Konopacka, A. Alien crustacea in polish waters—Amphipoda. Aquat. Invas. 2, 25–38. https://doi.org/10.3391/ai.2007.2.1.3 (2007).
    Article  Google Scholar 

    18.
    Kontula, T. & Väinölä, R. Postglacial colonization of Northern Europe by distinct phylogeographic lineages of the bullhead, Cottus gobio. Mol. Ecol. 10, 1983–2002. https://doi.org/10.1046/j.1365-294X.2001.01328.x (2001).
    CAS  Article  PubMed  Google Scholar 

    19.
    Mateus, C. S., Almeida, P. R., Mesquita, N., Quintella, B. R. & Alves, M. J. European lampreys: new insights on postglacial colonization, gene flow and speciation. PLoS ONE 11, 1–22. https://doi.org/10.1371/journal.pone.0148107 (2016).
    CAS  Article  Google Scholar 

    20.
    Jażdżewski, K. Range extensions of some gammaridean species in European inland waters caused by human activity. 10–16 (1980).

    21.
    Bij de Vaate, A., Jażdżewski, K., Ketelaars, H. A. M., Gollasch, S. & Van der Velde, G. Geographical patterns in range extension of Ponto-Caspian macroinvertebrate species in Europe. Can. J. Fish. Aquat. Sci. 59, 1159–1174. https://doi.org/10.1139/f02-098 (2002).
    Article  Google Scholar 

    22.
    Panov, V. E. et al. Assessing the risks of aquatic species invasions via European inland waterways: from concepts to environmental indicators. Integr. Environ. Assess. Manag. 5, 110–126. https://doi.org/10.1897/IEAM_2008-034.1 (2009).
    CAS  Article  PubMed  Google Scholar 

    23.
    Väinölä, R. et al. Global diversity of amphipods (Amphipoda; Crustacea) in freshwater. Hydrobiologia 595, 241–255. https://doi.org/10.1007/s10750-007-9020-6 (2008).
    Article  Google Scholar 

    24.
    Weiss, M. & Leese, F. Widely distributed and regionally isolated! Drivers of genetic structure in Gammarus fossarum in a human-impacted landscape. BMC Evol. Biol. 16, 153. https://doi.org/10.1186/s12862-016-0723-z (2016).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    25.
    Weigand, A. M., Michler-Kozma, D., Kuemmerlen, M. & Jourdan, J. Substantial differences in genetic diversity and spatial structuring among (cryptic) amphipod species in a mountainous river basin. Freshw. Biol. 65, 1641–1656. https://doi.org/10.1111/fwb.13529 (2020).
    CAS  Article  Google Scholar 

    26.
    Rachalewski, M., Banha, F., Grabowski, M. & Anastácio, P. M. Ectozoochory as a possible vector enhancing the spread of an alien amphipod Crangonyx pseudogracilis. Hydrobiologia 717, 109–117. https://doi.org/10.1007/s10750-013-1577-7 (2013).
    Article  Google Scholar 

    27.
    Peck, S. B. Amphipod dispersal in the fur of aquatic mammals. Can. F. Nat. 89, 181–182 (1975).
    Google Scholar 

    28.
    Sainte-Marie, B. A review of the reproductive bionomics of aquatic gammaridean amphipods: variation of life history traits with latitude, depth, salinity and superfamily. Hydrobiologia 223, 189–227. https://doi.org/10.1007/BF00047641 (1991).
    Article  Google Scholar 

    29.
    Rewicz, T., Grabowski, M., MacNeil, C. & Bącela-Spychalska, K. The profile of a ‘perfect’ invader—the case of killer shrimp, Dikerogammarus villosus. Aquat. Invas. 9, 267–288. https://doi.org/10.3391/ai.2014.9.3.04 (2014).
    Article  Google Scholar 

    30.
    Vader, W. & Tandberg, A. H. S. Gammarid amphipods (Crustacea) in Norway, with a key to the species. Fauna Nor. 39, 12–25. https://doi.org/10.5324/fn.v39i0.2873 (2019).
    Article  Google Scholar 

    31.
    Macdonald, K. S., Yampolsky, L. & Duffy, J. E. Molecular and morphological evolution of the amphipod radiation of Lake Baikal. Mol. Phylogenet. Evol. 35, 323–343. https://doi.org/10.1016/j.ympev.2005.01.013 (2005).
    CAS  Article  PubMed  Google Scholar 

    32.
    Grabowski, M., Wysocka, A. & Mamos, T. Molecular species delimitation methods provide new insight into taxonomy of the endemic gammarid species flock from the ancient Lake Ohrid. Zool. J. Linn. Soc. 181, 272–285. https://doi.org/10.1093/zoolinnean/zlw025 (2017).
    Article  Google Scholar 

    33.
    Jabłońska, A., Wrzesińska, W., Zawal, A., Pešić, V. & Grabowski, M. Long-term within-basin isolation patterns, different conservation units, and interspecific mitochondrial DNA introgression in an amphipod endemic to the ancient Lake Skadar system, Balkan Peninsula. Freshw. Biol. 65, 209–225. https://doi.org/10.1111/fwb.13414 (2020).
    CAS  Article  Google Scholar 

    34.
    Copilaş-Ciocianu, D. & Petrusek, A. The southwestern Carpathians as an ancient centre of diversity of freshwater gammarid amphipods: insights from the Gammarus fossarum species complex. Mol. Ecol. 24, 3980–3992. https://doi.org/10.1111/mec.13286 (2015).
    Article  PubMed  Google Scholar 

    35.
    Copilaş-Ciocianu, D. & Petrusek, A. Phylogeography of a freshwater crustacean species complex reflects a long-gone archipelago. J. Biogeogr. 44, 421–432. https://doi.org/10.1111/jbi.12853 (2017).
    Article  Google Scholar 

    36.
    Leuven, R. S. E. W. et al. The river Rhine: a global highway for dispersal of aquatic invasive species. Biol. Invas. 11, 1989–2008. https://doi.org/10.1007/s10530-009-9491-7 (2009).
    Article  Google Scholar 

    37.
    Kelly, D. W., Muirhead, J. R., Heath, D. D. & Macisaac, H. J. Contrasting patterns in genetic diversity following multiple invasions of fresh and brackish waters. Mol. Ecol. 15, 3641–3653. https://doi.org/10.1111/j.1365-294X.2006.03012.x (2006).
    CAS  Article  PubMed  Google Scholar 

    38.
    Panov, V. & Berezina, N. Invasive aquatic species of Europe. Distribution, impacts and management. Invas. Aquat. Species Eur. Distrib. Impacts Manag. https://doi.org/10.1007/978-94-015-9956-6 (2002).
    Article  Google Scholar 

    39.
    Csabai, Z. et al. Mass appearance of the Ponto-Caspian invader Pontogammarus robustoides in the River Tisza catchment: bypass in the southern invasion corridor?. Knowl. Manag. Aquat. Ecosyst. https://doi.org/10.1051/kmae/2020003 (2020).
    Article  Google Scholar 

    40.
    Rewicz, T., Wattier, R., Grabowski, M., Rigaud, T. & Bącela-Spychalska, K. Out of the Black sea: phylogeography of the invasive killer shrimp Dikerogammarus villosus across Europe. PLoS ONE 10, 1–20. https://doi.org/10.1371/journal.pone.0118121 (2015).
    CAS  Article  Google Scholar 

    41.
    Rewicz, T. et al. The killer shrimp, Dikerogammarus villosus, invading European Alpine Lakes: a single main source but independent founder events with an overall loss of genetic diversity. Freshw. Biol. 62, 1036–1051. https://doi.org/10.1111/fwb.12923 (2017).
    CAS  Article  Google Scholar 

    42.
    Jażdżewska, A. M. et al. Cryptic diversity and mtDNA phylogeography of the invasive demon shrimp, Dikerogammarus haemobaphes (Eichwald, 1841), in Europe. NeoBiota 57, 53–86. https://doi.org/10.3897/neobiota.57.46699 (2020).
    Article  Google Scholar 

    43.
    Jażdżewski, K. & Roux, A. L. Biogéographie de Gammarus roeseli Gervais en Europe, en particulier répartition en France et en Pologne (1988).

    44.
    Piscart, C. & Bollache, L. Crustacés amphipodes de surface : gammares d’eau douce.. Association Française de Limnologie, Introduction pratique à la systématique des organismes des eaux continentales de France (2012).

    45.
    Paganelli, D., Gazzola, A., Marchini, A. & Sconfietti, R. The increasing distribution of Gammarus roeselii Gervais, 1835: first record of the non-indigenous freshwater amphipod in the sub-lacustrine Ticino River basin (Lombardy, Italy). Bioinvas. Rec. 4, 37–41. https://doi.org/10.3391/bir.2015.4.1.06 (2015).
    Article  Google Scholar 

    46.
    Karaman, G. S. & Pinkster, S. Freshwater gammarus species from Europe, North Africa and adjacent regions of Asia (Crustacea-Amphipoda) Part II. Gammarus roeseli-group and related species. Bijdragen tot de dierkunde 57, 207–260. https://doi.org/10.1163/26660644-05702005 (1977).
    Article  Google Scholar 

    47.
    Moret, Y., Bollache, L., Wattier, R. & Rigaud, T. Is the host or the parasite the most locally adapted in an amphipod-acanthocephalan relationship? A case study in a biological invasion context. Int. J. Parasitol. 37, 637–644. https://doi.org/10.1016/j.ijpara.2006.12.006 (2007).
    Article  PubMed  Google Scholar 

    48.
    Copilaş-Ciocianu, D., Borza, P. & Petrusek, A. Extensive variation in the morphological anti-predator defense mechanism of Gammarus roeselii Gervais, 1835 (Crustacea:Amphipoda). Freshw. Sci. 39, 47–55. https://doi.org/10.1086/707259 (2020).
    Article  Google Scholar 

    49.
    Miller, B. J., von der Heyden, S. & Gibbons, M. J. Significant population genetic structuring of the holoplanktic scyphozoan Pelagia noctiluca in the Atlantic Ocean. Afr. J. Mar. Sci. 34, 425–430. https://doi.org/10.2989/1814232X.2012.726646 (2012).
    Article  Google Scholar 

    50.
    Brown, W. M., George, M. Jr. & Wilson, A. C. Rapid evolution of animal mitochondrial DNA. Genetics 76, 1967–1971. https://doi.org/10.1002/(sici)1097-4555(199706)28:6%3c433::aid-jrs125%3e3.3.co;2-5 (1979).
    CAS  Article  Google Scholar 

    51.
    Kázmér, M. Birth, life and death of the Pannonian Lake. Palaeogeogr. Palaeoclimatol. Palaeoecol. 79, 171–188. https://doi.org/10.1016/0031-0182(90)90111-J (1990).
    Article  Google Scholar 

    52.
    Hewitt, G. M. Post-glacial re-colonization of European biota. Biol. J. Linn. Soc. 68, 87–112. https://doi.org/10.1006/bijl.1999.0332 (1999).
    Article  Google Scholar 

    53.
    Rudolph, K., Coleman, C. O., Mamos, T. & Grabowski, M. Description and post-glacial demography of Gammarus jazdzewskii sp. nov. (Crustacea: Amphipoda) from Central Europe. Syst. Biodivers. 16, 587–603. https://doi.org/10.1080/14772000.2018.1470118 (2018).
    Article  Google Scholar 

    54.
    Copilaş-Ciocianu, D., Fišer, C., Borza, P. & Petrusek, A. Is subterranean lifestyle reversible? Independent and recent large-scale dispersal into surface waters by two species of the groundwater amphipod genus Niphargus. Mol. Phylogenet. Evol. 119, 37–49. https://doi.org/10.1016/j.ympev.2017.10.023 (2018).
    Article  PubMed  Google Scholar 

    55.
    Antal, L. et al. Phylogenetic evidence for a new species of Barbus in the Danube River basin. Mol. Phylogenet. Evol. 96, 187–194. https://doi.org/10.1016/j.ympev.2015.11.023 (2016).
    CAS  Article  PubMed  Google Scholar 

    56.
    Walker, M. J. C. Climatic changes in Europe during the last glacial/interglacial transition. Quat. Int. 28, 63–76. https://doi.org/10.1016/1040-6182(95)00030-M (1995).
    Article  Google Scholar 

    57.
    Pawłowski, D. et al. The response of flood-plain ecosystems to the Late Glacial and Early Holocene hydrological changes: a case study from a small Central European river valley. CATENA 147, 411–428. https://doi.org/10.1016/j.catena.2016.07.034 (2016).
    CAS  Article  Google Scholar 

    58.
    Notebaert, B. & Verstraeten, G. Sensitivity of West and Central European river systems to environmental changes during the Holocene: a review. Earth Sci. Rev. 103, 163–182. https://doi.org/10.1016/j.earscirev.2010.09.009 (2010).
    ADS  Article  Google Scholar 

    59.
    Gibling, M. R. River systems and the anthropocene: a late pleistocene and holocene timeline for human influence. Quaternary 1, 21. https://doi.org/10.3390/quat1030021 (2018).
    Article  Google Scholar 

    60.
    Gherardi, F. Biological invaders in inland waters: profiles, distribution, and threats. https://doi.org/10.1007/978-1-4020-6029-8 (2007).

    61.
    Jazdzewski, K., Konopacka, A. & Grabowski, M. Recent drastic changes in the gammarid fauna (Crustacea, Amphipoda) of the Vistula River deltaic system in Poland caused by alien invaders. Divers. Distrib. 10, 81–87. https://doi.org/10.1111/j.1366-9516.2004.00062.x (2004).
    Article  Google Scholar 

    62.
    Jourdan, J., Piro, K., Weigand, A. & Plath, M. Small-scale phenotypic differentiation along complex stream gradients in a non-native amphipod. Front. Zool. 16, 29. https://doi.org/10.1186/s12983-019-0327-8 (2019).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    63.
    Mauchart, P., Bereczki, C., Ortmann-Ajkai, A., Csabai, Z. & Szivák, I. Niche segregation between two closely related Gammarids (Crustacea, Amphipoda)—native vs. naturalised non-native species. Crustaceana 87, 1296–1314. https://doi.org/10.1163/15685403-00003355 (2014).
    Article  Google Scholar 

    64.
    Lagrue, C. et al. Interspecific differences in drift behaviour between the native Gammarus pulex and the exotic Gammarus roeseli and possible implications for the invader’s success. Biol. Invas. 13, 1409–1421. https://doi.org/10.1007/s10530-010-9899-0 (2011).
    Article  Google Scholar 

    65.
    Pöckl, M. & Humpesch, U. H. Intra- and inter-specific variations in egg survival and brood development time for Austrian populations of Gammarus fossarum and G. roeseli (Crustacea: Amphipoda). Freshw. Biol. 23, 441–455. https://doi.org/10.1111/j.1365-2427.1990.tb00286.x (1990).
    Article  Google Scholar 

    66.
    Pöckl, M. Effects of temperature, age and body size on moulting and growth in the freshwater amphipods Gammarus fossarum and G. roeseli. https://doi.org/10.1111/j.1365-2427.1992.tb00534.x (1992).

    67.
    Pöckl, M. Reproductive potential and lifetime potential fecundity of the freshwater amphipods Gammarus fossarum and G. roeseli in Austrian streams and rivers. Freshw. Biol. 30, 73–91. https://doi.org/10.1111/j.1365-2427.1993.tb00790.x (1993).
    Article  Google Scholar 

    68.
    Pöckl, M., Webb, B. W. & Sutcliffe, D. W. Life history and reproductive capacity of Gammarus fossarum and G. roeseli (Crustacea: Amphipoda) under naturally fluctuating water temperatures: a simulation study. Freshw. Biol. 48, 53–66. https://doi.org/10.1046/j.1365-2427.2003.00967.x (2003).
    Article  Google Scholar 

    69.
    Aguilera-Muñoz, F., Lafarga-Cruz, F. & Gallardo-Escárate, C. Molecular analysis in Chilean commercial gastropods based on 16S rRNA, COI and ITS1-5.8S rDNA-ITS2 sequences. Gayana (Concepción) 73, 17–27. https://doi.org/10.4067/s0717-65382009000100003 (2009).
    Article  Google Scholar 

    70.
    Alvarez, J. M. & Hoy, M. A. Evaluation of the ribosomal ITS2 DNA sequences in separating closely related populations of the Parasitoid Ageniaspis (Hymenoptera: Encyrtidae) article. Ann. Entomol. Soc. Am. https://doi.org/10.1603/0013-8746(2002)095 (2002).
    Article  Google Scholar 

    71.
    Wesson, D. M., McLain, D. K., Oliver, J. H., Piesman, J. & Collins, F. H. Investigation of the validity of species status of Ixodes dammini (Acari: Ixodidae) using rDNA. Proc. Natl. Acad. Sci. U. S. A. 90, 10221–10225. https://doi.org/10.1073/pnas.90.21.10221 (1993).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    72.
    Tang, J., Toè, L., Back, C. & Unnasch, T. R. Intra-specific heterogeneity of the rDNA internal transcribed spacer in the Simulium damnosum (Diptera: Simuliidae) complex. Mol. Biol. Evol. 13, 244–252. https://doi.org/10.1093/oxfordjournals.molbev.a025561 (1996).
    CAS  Article  PubMed  Google Scholar 

    73.
    Palandačić, A., Bravničar, J., Zupančić, P., Šanda, R. & Snoj, A. Molecular data suggest a multispecies complex of Phoxinus (Cyprinidae) in the Western Balkan Peninsula. Mol. Phylogenet. Evol. https://doi.org/10.1016/j.ympev.2015.05.024 (2015).
    Article  PubMed  Google Scholar 

    74.
    Vucić, M., Jelić, D., Žutinić, P., Grandjean, F. & Jelić, M. Distribution of Eurasian minnows (Phoxinus : Cypriniformes) in the Western Balkans. Knowl. Manag. Aquat. Ecosyst. 419, 11. https://doi.org/10.1051/kmae/2017051 (2018).
    Article  Google Scholar 

    75.
    Buj, I. et al. Peculiar occurrence of Cobitis bilineata Canestrini, 1865 and Sabanejewia larvata (De Filippi, 1859) (Cobitidae, Actinopteri) in the Danube River basin in Croatia. Fundam. Appl. Limnol. https://doi.org/10.1127/fal/2020/1272 (2020).
    Article  Google Scholar 

    76.
    Manning, J. T. Male discrimination and investment in Asellus aquaticus (L.) and A. meridianus Racovitsza (Crustacea: Isopoda). Behaviour 55(1–2), 1–14 (1975).
    CAS  Article  Google Scholar 

    77.
    Bollache, L. & Cézilly, F. Sexual selection on male body size and assortative pairing in Gammarus pulex (Crustacea: Amphipoda): field surveys and laboratory experiments. J. Zool. 264, 135–141. https://doi.org/10.1017/S0952836904005643 (2004).
    Article  Google Scholar 

    78.
    Cornet, S., Luquet, G. & Bollache, L. Influence of female moulting status on pairing decisions and size-assortative mating in amphipods. J. Zool. 286, 312–319. https://doi.org/10.1111/j.1469-7998.2011.00882.x (2012).
    Article  Google Scholar 

    79.
    Grabner, D. S. et al. Invaders, natives and their enemies: distribution patterns of amphipods and their microsporidian parasites in the Ruhr Metropolis, Germany. Parasites Vectors https://doi.org/10.1186/s13071-015-1036-6 (2015).
    Article  PubMed  PubMed Central  Google Scholar 

    80.
    Karaman, G. S. & Pinkster, S. Freshwater gammarus species from Europe, North Africa and adjacent regions of Asia (Crustacea-Amphipoda) Part I. Gammarus pulex—group and related species (1977).

    81.
    Karaman, G. S. & Pinkster, S. Freshwater gammarus species from Europe, North Africa and adjacent regions of Asia (Crustacea-Amphipoda). Part III. Gammarus balcanicus—group and related species (1987).

    82.
    Hillis, D. M. & Moritz, C. Molecular Systematics (Sinauer Associates Inc., Sunderland, 1996).
    Google Scholar 

    83.
    Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410. https://doi.org/10.1016/S0022-2836(05)80360-2 (1990).
    CAS  Article  PubMed  Google Scholar 

    84.
    Kearse, M. et al. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649. https://doi.org/10.1093/bioinformatics/bts199 (2012).
    Article  PubMed  PubMed Central  Google Scholar 

    85.
    Sequencher version 5.4.6 DNA sequence analysis software, Gene Codes Corporation, Ann Arbor, MI USA https://www.genecodes.com.

    86.
    Rozas, J. et al. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol. Biol. Evol. 34, 3299–3302. https://doi.org/10.1093/molbev/msx248 (2017).
    CAS  Article  PubMed  Google Scholar 

    87.
    Ratnasingham, S. & Hebert, P. D. N. The barcode of life data system. Mol. Ecol. Notes 7, 355–364. https://doi.org/10.1111/j.1471-8286.2006.01678.x (2007).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    88.
    Bouckaert, R. et al. BEAST 2: a software platform for bayesian evolutionary analysis. PLoS Comput. Biol. 10, 1–6. https://doi.org/10.1371/journal.pcbi.1003537 (2014).
    CAS  Article  Google Scholar 

    89.
    Bouckaert, R. R. & Drummond, A. J. bModelTest: Bayesian phylogenetic site model averaging and model comparison. BMC Evol. Biol. 17, 1–11. https://doi.org/10.1186/s12862-017-0890-6 (2017).
    Article  Google Scholar 

    90.
    Rambaut, A., Suchard, M. A., Xie, D. & Drummond, A. J. Tracer v1.6. Available at https://beast.bio.ed.ac.uk/Tracer (2014).

    91.
    Kumar, S., Stecher, G. & Tamura, K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874. https://doi.org/10.1093/molbev/msw054 (2016).
    CAS  Article  PubMed  Google Scholar 

    92.
    Leigh, J. W. & Bryant, D. POPART: full-feature software for haplotype network construction. Methods Ecol. Evol. 6, 1110–1116. https://doi.org/10.1111/2041-210X.12410 (2015).
    Article  Google Scholar 

    93.
    Tajima, F. Statistical Method for Testing the Neutral Mutation Hypothesis by DNA Polymorphism. (1989).

    94.
    Fu, Y. X. New statistical tests of neutrality for DNA samples from a population. Genetics 143, 557–570 (1996).
    CAS  PubMed  PubMed Central  Google Scholar 

    95.
    Excoffier, L. & Lischer, H. E. L. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10, 564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x (2010).
    Article  PubMed  Google Scholar 

    96.
    Copilaş-Ciocianu, D., Grabowski, M., Parvulescu, L. & Petrusek, A. Zoogeography of epigean freshwater Amphipoda (Crustacea) in Romania: fragmented distributions and wide altitudinal variability. Zootaxa 3893, 243. https://doi.org/10.11646/zootaxa.3893.2.5 (2014).
    Article  PubMed  Google Scholar  More

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    Water strider females use individual experience to adjust jumping behaviour to their weight within physical constraints of water surface tension

    Study animals
    Between June and August 2014, male and female Gerris latiabdominis were collected using insect nets from small ponds and an old swimming pool at Seoul National University, Seoul, South Korea. The number of water strider collected weekly varied depending on the current experimental requirements. In total, we collected near 100 individuals and used 62 of them in the experiments reported here. Collected water striders were housed in plastic containers (52 × 42 × 18 cm, 2–4 individuals/container) with aerated water, foam resting platforms, and two frozen large crickets per container per day. Each water strider’s thorax was marked with three unique color-coded dots using enamel paints. Females and males were housed separately.
    Experiments
    Effect of weight addition on the performance of first jumps
    Experimental design is graphically summarized in Fig. 1b (also see Supplementary Materials PART 4). To determine the effect of increase in body mass on the behaviour, we tested water striders in two conditions of the Additional weight treatment: weight-added (11 females and 16 males) and weight-not-added (20 females and 15 males). After measuring the weight with an Ohaus electronic scale with the precision of 0.1 mg, the water striders were randomly assigned to either of the treatment group. In weight-added group, a flat coiled aluminum wire (~ 7.5 mg weight in males, ~ 10.5 mg weight in females) was secured to the backs of water striders with a tiny drop of non-water soluble glue gel (applied only on top of thorax). Added weights caused an increase of body mass by about 50% (54.5% ± 9.2 (mean ± SD) in males and 52.8% ± 5.7 in females). The body weight of a male is about 70% of female body weight on average (similar based on median or average body weights). Preliminary theoretical calculations using the model of surface-tension dominated jumping3 suggested that an average female with the extra weight equivalent to the average male body mass would be able to jump and to achieve take-off velocity of about 0.75 m/s for the leg angular velocity of about 40 rad/s. However, based on our observations, when a male sits on the female’s back during copulation and mate guarding the male’s hindlegs are always on the water, probably adding to the support for the mating pair on the water surface. The tips of male midlegs can also be on the water surface, possibly also helping in support on the water surface. All evidence suggests that the male’s support on the water surface contributes to some extent to the forces maintaining the mating pair on the surface of water. Hence, the female does not perceive the full body weight of the mating male. Our preliminary trials with additional weight of different masses indicated that the weight similar to the male body mass is too heavy for the purpose of our experiments because some females were not able to stay on the surface for extended time periods. This was not observed for the extra weights used in our experiments.
    After the weight was added to the water strider, the animal was allowed to rest with 2–3 other individuals of the same sex in a container filled with water (20 × 14 × 10 cm). After three hours, the water strider was placed in a box where the 3-D slow motion movie of the jump was recorded (labeled as the First jump; see below for the details). In weight-not-added group the individuals were treated similarly and handled for similar duration but no extra weight (neither wire nor the glue) was put on their backs. Triggering repeated jumps successively many times in the small container in which they were filmed likely leads to changes in performance due to repeated jumps within relatively short time and due to accumulated effect of the heat of the lights needed for high speed filming. We decided to use the design in which we took one jump per individual. The final sample sizes differ between treatments because some movies were discarded at the analysis stage for technical reasons.
    Effect of jumping experience on adjustment of jumping performance
    In order to test the effect of individual’s experience on adjustments of jumping behaviour we subjected the males and females from the preceding First jump to two conditions of Jumping experience [JE] treatment: presence and absence of frequent jumping during a three-day period (Fig. 1). For three days following the filming of First jump, water striders were kept in groups of 3–4 individuals per container (20 × 14 × 10 cm; filled with aerated water) and fed two frozen crickets per day. Each container was assigned to either JE-present or JE-absent treatment. In the former, we used an aluminum wire bent in the shape of a hook to touch or poke the insect’s underside in order to trigger 3–5 jumps/hour over 5 h/day. Jumps provide individuals with repeated experience of their jumping performance and the opportunity to adjust jumping behaviour. In the latter, individuals were not exposed to these procedures. At the end of the three days, the jumps (Second jump) were recorded in the same manner as for First jump. Sample sizes (listed in caption to Fig. 3 and in Supplementary Table 7 in Supplementary Materials PART 4) differ between treatments because some movies were discarded for technical reasons (see below) and some animals escaped or died.
    High speed filming of jumps
    We used three synchronized high-speed cameras (FasTec Troubleshooter Model #: TS1000ME), with lens axes perpendicular to one another (Supplementary Fig. 2b in Supplementary Materials PART 4). Lights (Photon Super Energy Light, Aurora CCD-250 W, and PLTHINK Photo Light Think with Metal Halide bulbs) were placed directly opposite to each camera lens (Supplementary Fig. 2b). At the center of the setup was a 10 × 10 × 10 cm clear Plexiglas box filled with water. The jumps were invoked by an aluminum wire bent in the shape of a hook underneath the water surface. Jumps were recorded at 500 frames per second. Clips with insects that were accidentally pushed upward by the wire were excluded from the analyses. Examples of jumps extracted for the movies are shown in the Supplementary Movie.
    Variables extracted from the videos
    We tracked the locations of body parts of water striders frame by frame in a three dimensional x, y, z, coordinate system (x, y are horizontal axes, z-coordinates are on the vertical axis, and origin is located at the level of undisturbed water surface) using video tracking software MaxTRAQ 3D (Innovision Systems). We tracked three markers; body center (defined as point between midleg and hindlegs), right midleg dimple depth, and left midleg dimple depth. Dimple depth is the deepest point of water surface deflection under the pressure from a midleg. From this data we calculated upward (vertical) and forward (horizontal) body velocities. For each pair of consecutive frames, we calculated the raw upward velocity of body center (along the vertical axis z) by dividing the vertical shift of body center (vertical distance between z coordinates of body center in the two consecutive frames) by the duration (2 ms between frames in 500 fps movie). Then, we calculated smoothed vertical velocity (m/s) by using rolling three-point average of three successive velocities. In an analogical manner we calculated the values of smoothed horizontal velocity (m/s) during a jump. From the data we extracted four variables used in analyses:
    Angular leg speed (rad/s): Legs move downward as a result of downward angular femur movement powered by insect’s muscles, and the rotational rate of the leg downward movement is termed Angular leg speed (rad/s). To match the angular leg speed calculations in the theoretical model3, we calculated the Angular leg speed in several steps using empirical data and theoretical formulas from the existing model3. The coordinate system included vertical axis (z) with origin (z = 0) at the level of undisturbed water surface. First, for each frame we calculated average dimple depth as an average z from the left and right dimple depths’ z values, and the downward leg reach as the distance between body center’s z and the average dimple depth. Then, for each pair of consecutive frames, we calculated the downward velocity of dimple depth relative to body center (along the vertical axis z) by dividing the change in the downward leg reach between two consecutive frames by the duration (2 ms between frames in 500 fps movie). By using rolling three-point average from three successive downward velocities we obtained smoothed leg speed (m/s). Finally, we calculated the maximal downward speed of legs vs,max (m/s) as an average from the three largest smoothed velocity values. The downward Angular leg speed (ω) was calculated according to Yang et al.3 by approximation starting from the previously approved formula3 for the maximal downward speed of legs vs,max containing leg length ll: (v_{s,max } approx omega *left( { l_{l} – y_{i} } right)*sin left( {2omega t} right)) (yi indicates distance from the surface to insect body at rest and t indicates time during jump). See “Physical constraint from water surface: theoretical upper threshold of performance” below for more details about the model. The calculations resulted in the variable (Angular leg speed) that was directly relevant to the theoretical predictions of the optimal jumping behaviour3.
    Take-off angle (deg): We defined take-off angle (deg) as the angle of trajectory to the water surface when the water strider leaves the surface of water. Takeoff angle was calculated from the ratio of horizontal and vertical vectors of the smoothed body center velocities.
    Take-off velocity (m/s): Take-off velocity (m/s) is the vertical velocity of body center when the water strider leaves the surface of water. We determined the moment of leaving the water surface as the frame when legs disengage from the surface. Vertical velocity indicates how fast the animal removes itself from surface of water. A high take-off velocity is important when predators attack from underneath the water surface. This variable is a crucial component of the theoretical model of optimal jumping performance by water striders3.
    Meniscus breaking (binary): Sometimes jumping water striders break the water surface. When left or right midleg pierced the water surface by more than a quarter of its full leg length the jump was categorized as a jump with meniscus breaking-present. Otherwise the jump was categorized as a jump with meniscus breaking-absent.
    Statistical analyses
    Effect of weight addition on jumping performance—To analyze the effect of Additional weight on jumping performance of First jumps, we used Wilcoxon rank sum tests (Mann–Whitney test) to compare weight-added with weight-not-added groups for each sex separately. We used nonparametric statistical methods here because of small sample size that does not allow to confirm the parametric methods’ assumptions with high reliability (nevertheless the tests indicated that the parametric assumptions were probably met and in Supplementary Materials PART 1we also provide results from parametric comparisons: t-tests and Welch’s t-tests. In order to investigate whether Additional weight effect is statistically significantly different between sexes we switched to parametric analyses and run two-way ANOVA tests including the interaction effect between two independent variables (Additional weight and Sex) separately for the three dependent variables: Angular leg speed, Take-off angle and Take-off velocity.
    Effect of jumping experience on adjustments of jumping performance—For each individual, we calculated three indices of adjustment (change) in performance between First and Second jumps. For each of the three dependent variables, we subtracted the value at First jump from the value at Second jump (for analysis of Second jump solely—see Supplementary Materials PART 3). Linear regression model was used to investigate the effect of Jumping experience and Additional weight treatments on jumping adjustments. Because of the small sample sizes, estimates and 95% confidence intervals of regression coefficients were reported using nonparametric bootstrap procedure with 10,000 replications of each linear model (‘boot’ package in R).
    Meniscus breaking—To analyze the effect of Jumping experience and Additional weight treatments on the probability of breaking of the water surface (Meniscus breaking-present) we used Fisher’s exact test. To determine the effect of Meniscus breaking on Take-off velocity we used Wilcoxon rank sum test separately for males and females. All statistical analyses were performed using R (version 3.3.2;43).
    Physical constraint from water surface: theoretical upper threshold of performance
    During a water strider’s jump, the water surface can be pushed downward only so much before breaking. Thus, a theoretical upper threshold of performance exists. The mathematical model of surface tension dominated jumping3 allows to predict the moment of surface breaking and the optimal behaviour of vertically jumping water striders without surface breaking. The model contains a non-dimensional variable: ΩM1/2. Its value depends, among others, on the Angular leg speed used by water striders during jump and on morphology: body mass and midleg’s tibia and tarsus length—the leg parts on which water strider’s body is supported on the water surface. The theory predicts that for a given total length of midlegs there is a threshold value of ΩM1/2 above which surface breaking will occur and the jump will be inefficient. We determined if water striders used Angular leg speed values that resulted in theoretical values of ΩM1/2 below this critical threshold. In order to more precisely predict the theoretical threshold value of ΩM1/2we modified the original model3. The original model used a simple average length of all four legs (mid-legs and hind-legs) and did not reflect a difference between the length of hind and mid legs. We changed the original equation into systems of differential equations using information about midlegs and hindlegs separately. Modified predicted threshold values of ΩM1/2 were compared with empirically observed values of ΩM1/2in order to determine if the observed adjustments of leg speed by water striders lie within the theoretical limit of performance set by physical properties of water. We used the same parameters as in3 for, lc, capillary length, g, gravitational acceleration, ρ, density of water. Because of the short length of legs, we approximated C, flexibility factor, as 1. Downward angular velocity of leg rotation, ω, was calculated by approximation, (v_{s,max} approx omega {Delta }lsin left( {2omega t} right)). The averaged length of femur, tibia and tarsus were measured from 24 individuals of each sex in G. latiabdominis and yi, the distance from body center to the undisturbed water surface in the resting position of the water strider was measured from 4 movie clips of each sex. Measured variables were averaged (Supplementary Table 8 in Supplementary Materials Part 4) and used to determine lt, average length of tibia plus tarsus, ll, average leg length, and Δl = ll − yi, maximal reach of the leg. Note that, the average length of tibia plus tarsus of hind and mid legs, lth, ltm, and the average length of maximal reach of leg of hind and mid legs, Δlh, Δlm, can be represented as:

    $$l_{th} = 0.77l_{t} ,l_{tm} = 1.23l_{t} ,Delta l_{h} = 0.84Delta l,Delta l_{m} = 1.16Delta l$$

    $$ frac{{d^{2} H_{m} }}{{dleft( {omega t} right)^{2} }} + frac{4 cdot 1.23}{{{Omega }^{2} M}}H_{m} left( {1 – H_{m}^{2} /4} right)^{1/2} + frac{4 cdot 0.77}{{{Omega }^{2} M}}H_{h} left( {1 – H_{h}^{2} /4} right)^{1/2} – 2 cdot 1.16Lcos left( {2omega t} right) = 0, $$
    (1)

    $$ frac{{d^{2} H_{h} }}{{dleft( {omega t} right)^{2} }} + frac{4 cdot 1.23}{{{Omega }^{2} M}}H_{m} left( {1 – H_{m}^{2} /4} right)^{1/2} + frac{4 cdot 0.77}{{{Omega }^{2} M}}H_{h} left( {1 – H_{h}^{2} /4} right)^{1/2} – 2 cdot 0.84Lcos left( {2omega t} right) = 0, $$
    (2)

    where (H_{m} = h_{m} /l_{c} ) is the dimensionless dimple depth of mid legs (hm, dimple depth of mid legs), (H_{h} = h_{h} /l_{c}) is the dimensionless dimple depth of hind legs (h1, dimple depth of hind legs), ({Omega } = omega left( {l_{c} /g} right)^{1/2}) is the dimensionless angular velocity of leg rotation, (M = m/left( {rho l_{c}^{2} Cl_{t} } right)) is the dimensionless index of insect body mass (m, insect body mass), and (L = {Delta }l/l_{c}) is the dimensionless maximum downward reach of leg. The variable ΩM1/2 is calculated, as the name suggests, by multiplying the above-defined Ω by square root of M3. For a given L, the optimal value of ΩM1/2 for maximal take-off velocity is achieved when the maximal hm is equal to the critical depth, (sqrt 2 l_{C}), just before meniscus breaking. Wetted leg length, ls, was measured from 24 individuals of each sex in G. latiabdominis and initial height, yi, was measured from 12 recorded videos of females (6 individuals) and 9 recorded videos of males (5 individuals) (Supplementary Table 8 in Supplementary Materials Part 4). The ode45 function in Matlab was used to solve Eqs. (1) and (2) to get the optimal ΩM1/2 of male and female water striders (red lines in Fig. 4). More

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    Expansion of US wood pellet industry points to positive trends but the need for continued monitoring

    1.
    Solomon, S., Manning, M., Marquis, M. & Qin, D. Climate Change 2007-the Physical Science Basis: Working Group I Contribution to the Fourth Assessment Report of the IPCC Vol 4 (Cambridge university Press, 2007).
    2.
    Parliament, E. Directive 2009/28/EC of the European Parliament and of the Council of 23 April 2009 on the promotion of the use of energy from renewable sources and amending and subsequently repealing Directives 2001/77/EC and 2003/30/EC. Off. J. Eur. Union Belgium 20, 20 (2009).
    Google Scholar 

    3.
    Parliament, E. Directive (EU) 2018/2001 of the European Parliament and of the Council of 11 December 2018 on the promotion of the use of energy from renewable sources. Off. J. Eur Union Belgium 20, 2 (2018).
    Google Scholar 

    4.
    United Nations Climate Change Conference. Paris Agreement (2015).

    5.
    Eurostat. Supply, transformation and consumption of renewable energies: Annual data. Eurostat Website. https://ec.europa.eu/eurostat/web/energy/data/database (2019).

    6.
    European Commission. National renewable energy action plans 2020. https://ec.europa.eu/energy/en/topics/renewable-energy/national-renewable-energy-action-plans-2020 (2020).

    7.
    Camia, A. et al. Biomass production, supply, uses and flows in the European Union. 1–126 (2018) https://doi.org/10.2760/181536.

    8.
    Evans, A., Strezov, V. & Evans, T. J. Biomass Processing Technologies (CRC Press, Boca Raton, 2014). https://doi.org/10.1201/b17093.
    Google Scholar 

    9.
    Goerndt, M. E., Aguilar, F. X. & Skog, K. Resource potential for renewable energy generation from co-firing of woody biomass with coal in the Northern US. Biomass Bioenergy 59, 348–361 (2013).
    Article  Google Scholar 

    10.
    Spelter, H. & Toth, D. North America’s Wood Pellet Sector. USDA, Forest Products Laboratory. https://www.fs.usda.gov/treesearch/pubs/35060 (2009). https://doi.org/10.2737/FPL-RP-656.

    11.
    Eurostat. International trade, EU trade since 1988 by HS6. Product 440131. Eurostat Website. https://ec.europa.eu/eurostat/web/international-trade-in-goods/data/database (2019).

    12.
    Proskurina, S., Junginger, M., Heinimö, J., Tekinel, B. & Vakkilainen, E. Global biomass trade for energy—Part 2: Production and trade streams of wood pellets, liquid biofuels, charcoal, industrial roundwood and emerging energy biomass. Biofuels Bioprod. Biorefining 13, 371–387 (2019).
    CAS  Article  Google Scholar 

    13.
    Abt, K. L., Abt, R. C., Galik, C. S. & Skog, K. E. Effect of policies on pellet production and forests in the US South: A technical document supporting the forest service update of the 2010 RPA assessment. Gen. Tech. Rep. SRS-202 Asheville NC US Dep. Agric. For. Serv. South. Res. Stn. 202, 33 (2014).
    Google Scholar 

    14.
    Dale, V. H., Parish, E., Kline, K. L. & Tobin, E. How is wood-based pellet production affecting forest conditions in the southeastern United States?. For. Ecol. Manag. 396, 143–149 (2017).
    Article  Google Scholar 

    15.
    Singh, D., Cubbage, F., Gonzalez, R. & Abt, R. Locational determinants for wood pellet plants: A review and case study of North and South America. BioResources 11, 7928–7952 (2016).
    Google Scholar 

    16.
    U.S. Energy Information Administration (EIA). Monthly Densified Biomass Fuel Report. https://www.eia.gov/biofuels/biomass/#dashboard (2019).

    17.
    Birdsey, R. et al. Climate, economic, and environmental impacts of producing wood for bioenergy. Environ. Res. Lett. 13, 050201 (2018).
    ADS  Article  CAS  Google Scholar 

    18.
    Strange Olesen, A., Bager, L., Kittler, B., Price, W. & Aguilar, F. Environmental implications of increased reliance of the EU on biomass from the south east US. Brussels DG Environ. https://doi.org/10.2779/30897 (2015).
    Article  Google Scholar 

    19.
    Duden, A. S. et al. Modeling the impacts of wood pellet demand on forest dynamics in southeastern United States. Biofuels Bioprod. Biorefining 11, 1007–1029 (2017).
    CAS  Article  Google Scholar 

    20.
    Sedjo, R. & Tian, X. Does wood bioenergy increase carbon stocks in forests?. J. For. 110, 304–311 (2012).
    Google Scholar 

    21.
    de Oliveira Garcia, W., Amann, T. & Hartmann, J. Increasing biomass demand enlarges negative forest nutrient budget areas in wood export regions. Sci. Rep. 8, 5280 (2018).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    22.
    Searchinger, T. D. et al. Europe’s renewable energy directive poised to harm global forests. Nat. Commun. 9, 3741 (2018).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    23.
    Galik, C. S. & Abt, R. C. Sustainability guidelines and forest market response: An assessment of European Union pellet demand in the southeastern United States. GCB Bioenergy 8, 658–669 (2016).
    Article  Google Scholar 

    24.
    FORISK. Global Industrial Wood Pellet Demand Forecast and U.S. Wood Bioenergy Update: Q3 2017. https://forisk.com/blog/2017/08/08/global-industrial-wood-pellet-demand-forecast-u-s-wood-bioenergy-update-q3-2017/ (2017).

    25.
    Aguilar, F. X., Song, N. & Shifley, S. Review of consumption trends and public policies promoting woody biomass as an energy feedstock in the US. Biomass Bioenergy 35, 3708–3718 (2011).
    Article  Google Scholar 

    26.
    Robinson, G., McNulty, J. E. & Krasno, J. S. Observing the counterfactual? The search for political experiments in nature. Polit. Anal. 17, 341–357 (2009).
    Article  Google Scholar 

    27.
    Romijn, E. et al. Assessing change in national forest monitoring capacities of 99 tropical countries. For. Ecol. Manag. 352, 109–123 (2015).
    Article  Google Scholar 

    28.
    Cornwall, W. Is wood a green source of energy? Scientists are divided. Science (80) 355, 18–21 (2017).
    ADS  CAS  Article  Google Scholar 

    29.
    Glasenapp, S. & McCusker, A. Wood energy data: The joint wood energy enquiry. in Wood Energy in the ECE Region Data, Trends and Outlook in Europe, the Commonwealth of Independent States and North America 12 (United Nations Economic Commission for Europe, 2017).

    30.
    Wackernagel, M. & Yount, J. D. The ecological footprint: An indicator of progress toward regional sustainability. Environ. Monit. Assess. 51, 511–529 (1998).
    Article  Google Scholar 

    31.
    McCann, P. The Economics of Industrial Location: A Logistics-Costs Approach (Springer, Berlin, 2013).
    Google Scholar 

    32.
    Goerndt, M. E., Aguilar, F. X. & Skog, K. Drivers of biomass co-firing in US coal-fired power plants. Biomass Bioenergy 58, 158–167 (2013).
    Article  Google Scholar 

    33.
    Perez-Verdin, G., Grebner, D. L., Munn, I. A., Sun, C. & Grado, S. C. Economic impacts of woody biomass utilization for bioenergy in Mississippi. For. Prod. J. 58, 75–83 (2008).
    Google Scholar 

    34.
    European Commission Joint Research Centre. Renewable Energy—Recast to 2030 (RED II). https://ec.europa.eu/jrc/en/jec/renewable-energy-recast-2030-red-ii (2019).

    35.
    FORISK. U.S. Wood Bioenergy Database: Q1 2018. https://forisk.com/ (2018).

    36.
    U.S. International Trade Commission (USITC). Domestic Exports 2012–2018 for HS 44 and HS 440131. https://dataweb.usitc.gov/trade (2019).

    37.
    U.S. Department of Transportation (USDOT). Major Ports. https://data-usdot.opendata.arcgis.com/datasets/major-ports (2019).

    38.
    Blackman, A., Corral, L., Lima, E. S. & Asner, G. P. Titling indigenous communities protects forests in the Peruvian Amazon. Proc. Natl. Acad. Sci. 114, 4123–4128 (2017).
    CAS  PubMed  Article  Google Scholar 

    39.
    Mohebalian, P. M. & Aguilar, F. X. Beneath the canopy: Tropical forests enrolled in conservation payments reveal evidence of less degradation. Ecol. Econ. 143, 64–73 (2018).
    Article  Google Scholar 

    40.
    Burrill, E. A. et al. The Forest Inventory and Analysis Database: Database description and user guide version 8.0 for Phase 2. US Dep. Agric. For. Serv. 946, 20 (2018).
    Google Scholar 

    41.
    Guldin, R. W., King, S. L. & Scott, C. T. Vision for the Future of FIA: Paean to Progress, Possibilities, and Partners. Proceedings of Sixth Annual For. Invent. Anal. Symp. 2004 Sept. 21–24; Denver, CO. Gen. Tech. Rep. WO-70. Washington, DC U.S. Dep. Agric. For. Serv. 20090, 126 (2006).

    42.
    U.S. Department of Agriculture Forest Service. Forest Inventory and Analysis National Program. https://www.fia.fs.fed.us/tools-data/ (2019).

    43.
    Bechtold, W. A. & Patterson, P. L. The Enhanced Forest Inventory and Analysis Program—National Sampling Design and Estimation Procedures. Gen. Tech. Rep. SRS-80. Asheville, NC: US Department of Agriculture, Forest Service, Southern Research Station. 85 vol. 80. https://www.fs.usda.gov/treesearch/pubs/20371 (2015).

    44.
    Barbe, G. Methods of transporting timber in the southern United States. Rep. to Louisiana For. Prod. Dev. Cent. (1993).

    45.
    Ferraro, P. J. Counterfactual thinking and impact evaluation in environmental policy. New Dir. Eval. 2009, 75–84 (2009).
    Article  Google Scholar 

    46.
    Dundar, B., McGarvey, R. G. & Aguilar, F. X. Identifying Optimal Multi-state collaborations for reducing CO2 emissions by co-firing biomass in coal-burning power plants. Comput. Ind. Eng. 101, 403–415 (2016).
    Article  Google Scholar 

    47.
    Woodall, C. W. et al. An overview of the forest products sector downturn in the United States. For. Prod. J. 61, 595–603 (2011).
    Google Scholar 

    48.
    U.S. Drought Monitor. GIS Data Files. https://droughtmonitor.unl.edu/Data/GISData.aspx (2019).

    49.
    U.S. Department of Agriculture Forest Service. U.S. Forest Change Assessment Viewer ForWarn. https://forwarn.forestthreats.org/fcav2/ (2019).

    50.
    Fisher, M., Chaudhury, M. & McCusker, B. Do forests help rural households adapt to climate variability? Evidence from Southern Malawi. World Dev. 38, 1241–1250 (2010).
    Article  Google Scholar 

    51.
    Wooldridge, J. M. Econometric Analysis of Cross Section and Panel Data (MIT Press, London, 2010).
    Google Scholar 

    52.
    Millo, G. & Piras, G. splm: Spatial panel data models in R. J. Stat. Softw. 47, 1–38 (2012).
    Article  Google Scholar 

    53.
    Kapoor, M., Kelejian, H. H. & Prucha, I. R. Panel data models with spatially correlated error components. J. Econom. 140, 97–130 (2007).
    MathSciNet  MATH  Article  Google Scholar 

    54.
    Baltagi, B. Econometric Analysis of Panel Data (Wiley, Oxford, 2008).
    Google Scholar 

    55.
    Hausman, J. A. Specification tests in econometrics. Econometrica 46, 1251 (1978).
    MathSciNet  MATH  Article  Google Scholar 

    56.
    Crouchet, S. E., Jensen, J., Schwartz, B. F. & Schwinning, S. Tree mortality after a hot drought: Distinguishing density-dependent and -independent drivers and why it matters. Front. For. Glob. Chang. 2, 21 (2019).
    Article  Google Scholar 

    57.
    European Commission. Directorate General for Energy. https://ec.europa.eu/energy/en/topics/renewable-energy/biomass (2019).

    58.
    European Commission. Memo: The Revised Renewable Energy Directive. https://ec.europa.eu/energy/sites/ener/files/documents/technical_memo_renewables.pdf (2016).

    59.
    The Sustainable Biomass Program. Standards. https://sbp-cert.org/documents/standards-documents/standards (2015).

    60.
    Stephens, S. L. et al. The effects of forest fuel-reduction treatments in the United States. Bioscience 62, 549–560 (2012).
    Article  Google Scholar 

    61.
    Berger, A. L. et al. Ecological impacts of energy-wood harvests: Lessons from whole-tree harvesting and natural disturbance. J. For. 111, 139–153 (2013).
    Google Scholar 

    62.
    Janowiak, M. & Webster, C. Promoting ecological sustainability in woody biomass harvesting. J. For. 108, 16–23 (2010).
    Google Scholar 

    63.
    Powers, R. F. et al. The North American long-term soil productivity experiment: Findings from the first decade of research. For. Ecol. Manag. 220, 31–50 (2005).
    Article  Google Scholar 

    64.
    Parliament, E. Commission Delegated Regulation (EU) 2019/807 of 13 March 2019 supplementing Directive (EU) 2018/2001 of the European Parliament and of the Council as regards the determination of high indirect land-use change-risk feedstock for which a significant expans. Off. J. Eur Union Belgium 20, 20 (2019).
    Google Scholar 

    65.
    Hanssen, S. V., Duden, A. S., Junginger, M., Dale, V. H. & van der Hilst, F. Wood pellets, what else? Greenhouse gas parity times of European electricity from wood pellets produced in the south-eastern United States using different softwood feedstocks. GCB Bioenergy 9, 1406–1422 (2017).
    CAS  Article  Google Scholar 

    66.
    Wang, W., Dwivedi, P., Abt, R. & Khanna, M. Carbon savings with transatlantic trade in pellets: Accounting for market-driven effects. Environ. Res. Lett. 10, 114019 (2015).
    ADS  Article  Google Scholar 

    67.
    U.S. Energy Information Administration (EIA). Monthly Energy Review: Renewable Energy Consumption: Electric power sector (Wood Energy Consumed by the Electric Power Sector). https://www.eia.gov/totalenergy/data/monthly/#renewable (2019).

    68.
    Sedjo, R. A. The biomass crop assistance program (BCAP): Some implications for the forest industry. SSRN Electron. J. 20, 10–22. https://doi.org/10.2139/ssrn.1581551 (2010).
    Article  Google Scholar 

    69.
    Evans, A. M., Perschel, R. T. & Kittler, B. A. Overview of forest biomass harvesting guidelines. J. Sustain. For. 32, 89–107 (2013).
    Article  Google Scholar 

    70.
    Flach, B., Lieberz, S. & Bolla, S. Report: Biofuels Annual. US Foreign Agricultural Service. https://apps.fas.usda.gov/newgainapi/api/Report/DownloadReportByFileName?fileName=BiofuelsAnnual_TheHague_EuropeanUnion_06-29-2020.(2020).

    71.
    European Environment Agency. Renewable Energy in Europe: Key for Climate Objectives, But Air Pollution Needs Attention. https://www.eea.europa.eu/themes/energy/renewable-energy/renewable-energy-in-europe-key (2019).

    72.
    U.S. Energy Information Administration (EIA). Annual Energy Outlook 2018 Table: Renewable Energy Generation by Fuel Case: Reference Case|Region: United States. https://www.eia.gov/outlooks/aeo/data/browser/#/?id=67-AEO2018&linechart=~ref2018-d121317a.9-67-AEO2018.3-0 (2018).

    73.
    U.S. Environmental Protection Agency (EPA). Emissions and Generation Resource Integrated Database (eGRID). https://www.epa.gov/energy/emissions-generation-resource-integrated-database-egrid. (2019).

    74.
    National Conference of State Legislatures. State Renewable Portfolio Standards and Goals. https://www.ncsl.org/research/energy/renewable-portfolio-standards.aspx (2018).

    75.
    Shifley, S. R. et al. Five anthropogenic factors that will radically alter forest conditions and management needs in the Northern United States. For. Sci. 60, 914–925 (2014).
    Article  Google Scholar 

    76.
    Wear, D. N. & Greis, J. G. The Southern Forest Futures Project : Summary report/David N. Wear and John G. Greis. General technical report SRS: 168 vol. 168. https://proxy-remote.galib.uga.edu/login?url=https://search.ebscohost.com/login.aspx?direct=true&db=edsgpr&AN=gprocn839703115&site=eds-live. https://www.srs.fs.fed.us/pubs/gtr/gtrsrs168.pdf (2012).

    77.
    Ruta, G. Monitoring Environmental Sustainability (World Bank, Geneva, 2010). https://doi.org/10.1596/27445.
    Google Scholar 

    78.
    European Commission. A Sustainable Bioeconomy for Europe: Strengthening the Connection Between Economy, Society and the Environment. https://ec.europa.eu/research/bioeconomy/pdf/ec_bioeconomy_strategy_2018.pdf (2018).

    79.
    Council of the European Communities & Commission of the European Communities. Treaty on European Union-Maastricht Treaty. 253 (1993).

    80.
    European Union. Treaty of Amsterdam. 144 (1997).

    81.
    Dyer, J. M. Revisiting the deciduous forests of eastern North America. Bioscience 56, 341–352 (2006).
    Article  Google Scholar 

    82.
    U.S. Energy Information Administration. From EIA-860 Detailed Data with Previous form Data (EIA-860A/860B). https://www.eia.gov/electricity/data/eia860/ (2019).

    83.
    U.S. Energy Information Administration. Form EIA-923 Detailed Data with Previous form Data (EIA-906/920). https://www.eia.gov/electricity/data/eia923/ (2019).

    84.
    Gray, J. A., Bentley, J. W., Cooper, J. A. & Wall, D. J. United States Department of Agriculture Southern Pulpwood Production, 2016. e-Resource Bulletin SRS–222. Asheville, NC: U.S. Department of Agriculture Forest Service, Southern Research Station https://www.fs.usda.gov/treesearch/pubs/56531 (2018).

    85.
    Piva, R. J., Bentley, J. W. & Hayes, S. W. National pulpwood production, 2010. Resour. Bull. NRS-89. Newtown Square, PA: U.S. Department of Agriculture, Forest Service, Northern Research Station https://www.fs.usda.gov/treesearch/pubs/45928 (2014). https://doi.org/10.2737/NRS-RB-89.

    86.
    Prestemon, J. et al. Locations of Wood-Using Mills in the Continental U.S. https://www.srs.fs.usda.gov/econ/data/mills/ (2005).

    87.
    Johnson, T. G. & Steppleton, C. D. United States Department of Agriculture Southern Pulpwood Production, 2005. Resour. Bull. SRS-116. Asheville, NC: U.S. Department of Agriculture Forest Service, Southern Research Station. https://www.fs.usda.gov/treesearch/pubs/27728 (2007).

    88.
    Johnson, T. G., Steppleton, C. D. & Bentley, J. W. United States Department of Agriculture Southern Pulpwood Production, 2008. Resour. Bull. SRS–165. Asheville, NC: U.S. Department of Agriculture Forest Service, Southern Research Station. https://www.fs.usda.gov/treesearch/pubs/34565 (2010).

    89.
    Bentley, J. W. & Steppleton, C. D. Southern pulpwood production, 2011. Resour. Bull. SRS-RB-194. Asheville, NC: U.S. Department of Agriculture Forest Service, Southern Research Station. https://www.fs.usda.gov/treesearch/pubs/43626 (2013).

    90.
    Gray, J. A., Bentley, J. W., Cooper, J. A. & Wall, D. J. United States Department of Agriculture Southern Pulpwood Production, 2014. e-Resource Bulletin SRS–219. Asheville, NC: U.S. Department of Agriculture Forest Service, Southern Research Station. https://www.fs.usda.gov/treesearch/pubs/56235 (2018).

    91.
    U.S. Census Bureau. Cartographic Boundary Files. https://www.census.gov/geographies/mapping-files/time-series/geo/carto-boundary-file.html (2019).

    92.
    U.S. Census Bureau. County Population Totals. https://www.census.gov/data/tables/time-series/demo/popest/2010s-counties-total.html (2020).

    93.
    R Core Team. R: A Language and Environment for Statistical Computing. https://www.r-project.org/ (2019).

    94.
    Pebesma, E. Simple features for R: Standardized support for spatial vector data. R J. 10, 439 (2018).
    Article  Google Scholar 

    95.
    Flowerdew, R. & Green, M. Areal interpolation and types of data. In Spatial Analysis and GIS (eds Fotheringham, S. & Rogerson, P.) 73–75 (CRC Press, Boca Raton, 2014).
    Google Scholar 

    96.
    Goerndt, M. E., Wilson, B. T. & Aguilar, F. X. Comparison of small area estimation methods applied to biopower feedstock supply in the Northern US region. Biomass Bioenergy 121, 64–77 (2019).
    Article  Google Scholar  More

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    A rigorous assessment and comparison of enumeration methods for environmental viruses

    Bacteriophages
    Four lytic E. coli-specific phages were used in the present study: MS2 (DSM 13767), T4 (DSM 4505), T7 (DSM 4623), and ϕX174 (DSM 4497). The genomic and structural properties of the phages as well as their bacterial hosts are listed in Table 2. For preparation of the virus isolate stocks, the respective bacterial host was grown in sterile LB medium (LB broth Miller, Sigma-Aldrich, St. Louis, Missouri) until an optical density of 0.3 measured at 600 nm was reached, then inoculated with phages at a virus-to-bacteria-ratio of 0.1, followed by overnight incubation. Remaining bacterial cells were killed by the addition of 1/10 volume of chloroform for 1 h. After separation from the bacterial cell debris, virus stocks were filtered with 0.22 µm syringe filters (Millex-GP, Merck-Millipore, Billerica, Massachusetts) and filtration was repeated prior preparation of samples for measurements.
    Environmental samples
    Environmental samples were collected from four different aquatic habitats: the income water tank of a wastewater treatment plant (Gut Großlappen, Munich, Germany), an on-site groundwater collection well (48°13′25.8″ N 11°35′45.4″ E, Munich, Germany), a lake (Feldmochinger See; 48°12′56.0″ N 11°30′49.4″ E, Munich, Germany), and a river (Isar; 48°32′59.3″ N, 12°10′42.4″ E, Landshut, Germany). To remove particles the size of bacteria and larger, all water samples were filtered with 0.22 µm syringe filters (Millex-GP). Measurements with flow cytometer and nanoparticle tracking analysis were performed simultaneously and on the sampling day. Quantification with epifluorescence microscopy as well as DNA extraction was conducted on the next day. Samples were stored in 4 °C.
    Additionally, a mixed water sample (lake and wastewater) with an approximate concentration of 108 virus-like particles per mL (VLP mL–1) was prepared. This sample was spiked with 1× 108, 5× 108 and 1× 109 T4 particles mL−1. Before the addition, phage T4 stock has been quantified with qPCR.
    Viral quantification
    All measurements were performed in biological and technical duplicates.
    Plaque assay (PA)
    The PA was performed using a soft agar overlay technique as described elsewhere24. Briefly, 0.5 mL of appropriate dilutions of phages were mixed with an equal volume of fresh cultures of the corresponding hosts, grown overnight (incubated in LB medium at 37 °C until an optical density of 0.3 measured at 600 nm was reached). The phage-bacteria-suspension was mixed with 3 mL warm soft agar (0.75% w/v agar and 2.5% w/v LB) and gently poured on a petri dish already containing an LB agar layer (1.5% w/v agar and 2.5% w/v LB) in biological and technical replicates. Upon solidification, the petri dishes were incubated bottom up for overnight at 37 °C. After 15–20 h, depending on the bacterial growth efficiency, the plaques formed were manually counted and the phage titers as plaque-forming units per mL (PFU mL–1) were calculated.
    Flow cytometry (FCM)
    All samples were prepared as described previously with some adaptations14. We decided on these modifications based on the publications of Tomaru and Nagasaki (2007) and Brum and colleagues (2013). More precisely, samples were not fixed with glutaraldehyde after sampling as this may decrease the fluorescence intensity as well as the viral counts. Tomaru and Nagasaki concluded, that a fixation does not necessarily improve the staining ability of the virus particles20. Besides, our samples were measured immediately on the day of sampling, thus a preservation of the viral particles was not necessary. Another step recommended by Brussaard (2004) we did not follow is the flash freezing of the viral sample in liquid nitrogen. It has been shown that nitrogen fixation hampers the preparation procedure for TEM resulting inter alia in morphology changes25. To what extent particles would be enumerated correctly after fixation and nitrogen treatment with nanoparticle tracking analysis where particle integrity would certainly play a role during the enumeration process, is also debatable. As consequence, we decided, to omit this step in order to maintain a consistent sample handling and accomplish comparable conditions for all methods.
    In brief, samples were diluted appropriately with sterile, filtered PBS buffer (0.02 µm Anotop 25 syringe filter, Whatman, Maidstone, UK; Sigma Aldrich) to fulfill the instrument’s optimal concentration requirements of approximately 106 VLP mL–1 (Table 1). Fluorescent TRUCOUNT beads (BD, Becton, Dickinson and Company, Franklin Lakes, New Jersey) were added to each sample as an internal reference. The samples were stained with 1 × SYBR gold nucleic acid stain (Thermo Fisher, Waltham, Massachusetts) and incubated either for 10 min at 80 °C (FCM80) or for 1 h at 30 °C (FCM30) prior to measurement. Tomaru & Nagasaki recommended an incubation at room temperature, as higher temperatures reduced the viral counts. We chose therefore two staining temperatures, one at 80 °C, following the suggestion of Brussaard14 and one at 30 °C, following the reference of Tomaru & Nagasaki20.
    All samples were measured with a FC500 flow cytometer equipped with an air-cooled 488 nm Argon ion laser (Beckman Coulter, Brea, California) in biological and technical replicates. Analysis and evaluation of the samples was performed using StemCXP Cytometer software (v2.2).
    Nanoparticle tracking analysis (NTA)
    Viral isolate samples were diluted appropriately with sterile phage buffer (10 mM Tris [pH 7.5], 10 mM MgSO4, and 0.4% w/v NaCl) to obtain the optimal concentration range of 107–109 VLP mL–1 (Table 1). Afterwards, samples were either untreated or stained with 1 × SYBR gold for 10 min at 80 °C or 1 h at 30 °C (NTA80 or NTA30, respectively). Each sample was injected manually into the machine’s specimen chamber with a sterile 1 mL syringe (Braun, Melsungen, Germany), and measured three times for 20 sec at room temperature in three independent preparations. Samples were measured using a NanoSight NS300 (Malvern Pananalytical Ltd., Malvern, United Kingdom) equipped with a B488 nm laser module and a sCMOS camera, following the manufacturer’s protocol. Analysis was performed with the NTA 3.1 Analytical software (release version build 3.1.45).
    Epifluorescence microscopy (EPI)
    Staining of the samples was carried out as described by Patel et al.26. Briefly, all samples were diluted appropriately with 0.02 µm filtered 1 × TE buffer (pH 7.5, AppliChem, Darmstadt, Germany) to a concentration of 107 particles mL–1. For environmental samples with lower concentrations, a volume of 10 mL was used.
    Then, 1 mL of each diluted sample (10 mL of environmental samples) was passed through a 0.02 µm Anodisc filter (Whatman) in duplicates. After complete desiccation, the filter was stained using a drop of 2 × SYBR gold dye (Thermo Fisher) with the virus side up, and incubated at room temperature for 15 min in the dark. Stained filters were mounted on a glass slide with 20 µL antifade solution (Thermo Fisher). Slides were analyzed using an Axiolab fluorescence microscope (Carl Zeiss, Oberkochen, Germany) equipped with a 488 nm laser. A camera was used to take ten pictures per sample, which were analyzed using ImageJ (version 1.50i). Numbers of particles on the whole filter were calculated by multiplying the counts with the quotient of the area of the filter by area of the pictures.
    Quantitative real-time PCR (qRT-PCR)
    Prior to the DNA extraction 1 mL of sample has been treated with DNase as described previously with a modified incubation procedure for one hour at 37 °C27. The DNA extraction has been conducted from the complete volume after DNase treatment using the Wizard® PCR Preps DNA Purification Resin and Minicolumns (Promega, Madison, Wisconsin) as previously described28. RNA was extracted with a QIAmp MinElute Virus Spin Kit (total volume of 1 mL sample) (Qiagen, Hilden, Germany) and cDNA was synthesized using a DyNAmo cDNA Synthesis Kit (Thermo Fisher) according to the manufacturers protocols. For all samples, DNA or RNA was isolated in duplicates.
    T4 was quantified using primers amplifying a 163 bp region of the gp18 tail protein (T4F 5′-AAGCGAAAGAAGTCGGTGAA-3′ and T4R 5′-CGCTGTCATAGCAGCTTCAG-3′)29. For T7, primers amplifying a 555 bp segment of gene 1 (T7_4453F 5′-CTGTGTCAATGTTCAACCCG-3′ and T7_5008R 5 ‘-GTGCCCAGCTTGACTTTCTC-3′)30. ϕX174 was quantified using primers specific for the capsid protein F (ϕX174F 5′-ACAAAGTTTGGATTGCTACTGACC-3′ and ϕX174R 5′-CGGCAGCAATAAACTCAACAGG-3′) resulting in a 122 bp fragment31. For MS2, primers amplifying a 314-bp fragment (MS2_2717F 5′-CTGGGCAATAGTCAAA-3′ and MS2_3031R 5′-CGTGGATCTGACATAC-3′) were used32. Quantitative PCR was performed in a total volume of 20 µL consisting of 10 µL Brilliant III Ultra-Fast QPCR Master Mix (Agilent, Santa Clara, California), 5 µL DNA template or PCR-grade water as a negative control, as well as the following optimized primer concentrations (supporting information): 0.5 µM primers T4F and T4R, 0.8 µM primers T7_4453F and T7_5008R, 0.6 µM primers ϕX174F and ϕX174R, or 0.3 µM primers MS2_2717F and MS2_3031R, respectively. The amplifications were run on a Mx3000P qPCR system (FAM/SYBR® Green I filter [492 nm–516 nm], OS v7.10, Stratagene, San Diego, California) with the following cycling conditions: T4: 95 °C for 10 min, (95 °C for 15 sec, 60 °C for 1 min, 72 °C for 1 min) for a total of 45 cycles, T7: 95 °C for 12 min, (95 °C for 30 sec, 58 °C for 30 sec, 72 °C for 1 min) for a total of 30 cycles, ϕX174: 94 °C for 3 min, (94 °C for 15 sec, 60 °C for 1 min) for a total of 40 cycles, and MS2: 95 °C for 10 min, (95 °C for 15 sec, 50 °C for 30 sec, 72 °C for 30 sec) for a total of 45 cycles. Each replicate was measured four times. Analysis of the melting curves confirmed the specificity of the chosen primer as no variations compared to the standard melting curves could be observed. Standard curves were prepared using the appropriate dilutions of gblocks gene fragments (IDT, Coralville, Iowa) of the respective viral DNA in PCR-grade water (supporting information, Tables S1 and S2). Data analysis was performed using the manufacturer’s MxPro Mx3000P software (v4.10).
    TEM preparation
    Although TEM may be used for quantification, only the virus morphology and integrity upon applying the staining conditions were monitored. Therefore, the phages MS2 and T7 were either incubated for 10 min at 80 °C or further processed without any temperature treatment. Ten µL of the sample were then applied to the carbon side of a carbon-coated copper grid. Excessive water was blotted dry with a filter paper and washed two times with double-distilled water. After each washing step grids were again blotted dry onto a filter paper before negative staining with 2% uranyl acetate for 20 sec. The staining liquid was blotted onto a filter paper and the grids were air-dried as described previously33. Transmission electron microscopy was carried out using a Zeiss EM 912 with an integrated OMEGA filter in zero-loss mode. The acceleration voltage was set to 80 kV and images were recorded using a Tröndle 2 k × 2 k slow-scan CCD camera (Tröndle Restlichtverstärker Systeme, Moorenweis, Germany).
    Sample stability test
    In order to substantiate our decision of omitting a fixative step for FCM measurements and to confirm a certain stability of the virus concentration over a short time range (few days), phage T4 and wastewater samples were measured with FCM at time 0, after 24 h and after 48 h. The samples were either kept in 4 °C or were fixed with 0.5% glutaraldehyde for 30 min in 4 °C followed by freezing in liquid nitrogen with adjacent storage at -80 °C, as suggested by Brussaard (2004). At each time point, samples were prepared for FCM as described above with two different staining procedures (30 °C and 80 °C). Additionally, a fixed T4 phage sample was prepared for NTA measurements in the same way in order to test the usability of glutaraldehyde fixation. For phage T4, measurements of the 4 °C, unfixed samples were mostly slightly higher compared to the fixed samples (Fig. S6a,b). Comparing the initial quantification with the results after 48 h, the decrease in counted particles was minor. For the wastewater samples, viral numbers of the unfixed samples were marginally lower, however, a general decline in particle numbers over time could be observed (Fig. S6c,d). This decline was in all cases less than one order of magnitude. As both, fixed and unfixed samples declined only to a small extent and no trend of a stronger decrease of viral particles in the unfixed samples could be observed, omitting the fixation with glutaraldehyde and liquid nitrogen is not supposed to have a wide influence on the enumeration within 48 h.
    Statistical analysis
    Statistical analysis was carried out in R (v3.4.3) and RStudio (v1.1.383). Data were log transformed and analysis of variance (ANOVA) was conducted. Normal distribution of data was confirmed by density plots and quantile–quantile plots; homogeneity of variances was confirmed with Levene’s test. Afterwards, multiple pairwise comparisons were calculated with a post-hoc Tukey honest significant differences test. In addition, similarities in viral isolate quantification methods were assessed using principal coordinate analysis. More