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    Self-disseminating vaccines to suppress zoonoses

    1.
    Redding, D. W., Moses, L. M., Cunningham, A. A., Wood, J. & Jones, K. E. Environmental-mechanistic modelling of the impact of global change on human zoonotic disease emergence: a case study of Lassa fever. Methods Ecol. Evol. 7, 646–655 (2016).
    Google Scholar 
    2.
    McCormick, J. B. & Fisher-Hoch, S. P. in Arenaviruses I: The Epidemiology, Molecular and Cell Biology of Arenaviruses — Current Topics in Microbiology and Immunology Vol. 262 (ed. Oldstone, M. B. A.) 75–109 (Springer, 2002).

    3.
    Jonsson, C. B., Figueiredo, L. T. M. & Vapalahti, O. A global perspective on hantavirus ecology, epidemiology, and disease. Clin. Microbiol. Rev. 23, 412–441 (2010).
    CAS  PubMed  PubMed Central  Google Scholar 

    4.
    Edson, D. et al. Routes of Hendra virus excretion in naturally-infected flying-foxes: implications for viral transmission and spillover risk. PLoS ONE 10, e0140670 (2015).
    PubMed  PubMed Central  Google Scholar 

    5.
    Luby, S. P., Gurley, E. S. & Jahangir Hossain, M. Transmission of human infection with Nipah virus. Clin. Infect. Dis. 49, 1743–1748 (2009).
    PubMed  PubMed Central  Google Scholar 

    6.
    Georgiou, G. et al. Display of heterologous proteins on the surface of microorganisms: from the screening of combinatorial libraries to live recombinant vaccines. Nat. Biotechnol. 15, 29–34 (1997).
    CAS  PubMed  Google Scholar 

    7.
    Leitner, W. W., Ying, H. & Restifo, N. P. DNA and RNA-based vaccines: principles, progress and prospects. Vaccine 18, 765–777 (1999).
    CAS  PubMed  PubMed Central  Google Scholar 

    8.
    Pardi, N., Hogan, M. J., Porter, F. W. & Weissman, D. mRNA vaccines — a new era in vaccinology. Nat. Rev. Drug Discov. 17, 261–279 (2018).
    CAS  PubMed  PubMed Central  Google Scholar 

    9.
    Rollier, C. S., Reyes-Sandoval, A., Cottingham, M. G., Ewer, K. & Hill, A. V. S. Viral vectors as vaccine platforms: deployment in sight. Curr. Opin. Immunol. 23, 377–382 (2011).
    CAS  PubMed  Google Scholar 

    10.
    Ferretti, L. et al. Quantifying SARS-CoV-2 transmission suggests epidemic control with digital contact tracing. Science 368, eabb6936 (2020).
    CAS  PubMed  PubMed Central  Google Scholar 

    11.
    Morse, S. S. et al. Prediction and prevention of the next pandemic zoonosis. Lancet 380, 1956–1965 (2012).
    PubMed  PubMed Central  Google Scholar 

    12.
    Rupprecht, C. E., Hanlon, C. A. & Slate, D. in Control of Infectious Animal Diseases by Vaccination — Developments in Biologicals Vol. 119 (eds Schudel, A. & Lombard, M.) 173–184 (Karger, 2004).

    13.
    Bull, J. J., Smithson, M. W. & Nuismer, S. L. Transmissible viral vaccines. Trends Microbiol. 26, 6–15 (2018).
    CAS  PubMed  Google Scholar 

    14.
    Murphy, A. A., Redwood, A. J. & Jarvis, M. A. Self-disseminating vaccines for emerging infectious diseases. Expert Rev. Vaccines 15, 31–39 (2016).
    CAS  PubMed  Google Scholar 

    15.
    Shellam, G. R. The potential of murine cytomegalovirus as a viral vector for immunocontraception. Reprod. Fertil. Dev. 6, 401–409 (1994).
    CAS  PubMed  Google Scholar 

    16.
    Tyndale-Biscoe, C. H. Virus-vectored immunocontraception of feral mammals. Reprod. Fertil. Dev. 6, 281–287 (1994).
    CAS  PubMed  Google Scholar 

    17.
    Barcena, J. et al. Horizontal transmissible protection against myxomatosis and rabbit hemorrhagic disease by using a recombinant myxoma virus. J. Virol. 74, 1114–1123 (2000).
    CAS  PubMed  PubMed Central  Google Scholar 

    18.
    Torres, J. M. et al. First field trial of a transmissible recombinant vaccine against myxomatosis and rabbit hemorrhagic disease. Vaccine 19, 4536–4543 (2001).
    CAS  PubMed  Google Scholar 

    19.
    Angulo, E. & Barcena, J. Towards a unique and transmissible vaccine against myxomatosis and rabbit haemorrhagic disease for rabbit populations. Wildl. Res. 34, 567–577 (2007).
    CAS  Google Scholar 

    20.
    Nuismer, S. L. et al. Eradicating infectious disease using weakly transmissible vaccines. Proc. R. Soc. B 283, 20161903 (2016).
    PubMed  Google Scholar 

    21.
    Basinski, A. J., Nuismer, S. L. & Remien, C. H. A little goes a long way: weak vaccine transmission facilitates oral vaccination campaigns against zoonotic pathogens. PLoS Negl. Trop. Dis. 13, e0007251 (2019).
    PubMed  PubMed Central  Google Scholar 

    22.
    Basinski, A. J. et al. Evaluating the promise of recombinant transmissible vaccines. Vaccine 36, 675–682 (2018).
    CAS  PubMed  Google Scholar 

    23.
    Smithson, M. W., Basinki, A. J., Nuismer, S. L. & Bull, J. J. Transmissible vaccines whose dissemination rates vary through time, with applications to wildlife. Vaccine 37, 1153–1159 (2019).
    CAS  PubMed  PubMed Central  Google Scholar 

    24.
    Lecompte, E. et al. Mastomys natalensis and Lassa fever, West Africa. Emerg. Infect. Dis. 12, 1971–1974 (2006).
    PubMed  PubMed Central  Google Scholar 

    25.
    Olayemi, A. et al. New hosts of the Lassa virus. Sci. Rep. 6, 25280 (2016).
    CAS  PubMed  PubMed Central  Google Scholar 

    26.
    Douglass, R. J. et al. Longitudinal studies of Sin Nombre virus in deer mouse-dominated ecosystems of Montana. Am. J. Trop. Med. Hyg. 65, 33–41 (2001).
    CAS  PubMed  Google Scholar 

    27.
    Luis, A. D., Douglass, R. J., Mills, J. N. & Bjornstad, O. N. The effect of seasonality, density and climate on the population dynamics of Montana deer mice, important reservoir hosts for Sin Nombre hantavirus. J. Anim. Ecol. 79, 462–470 (2010).
    PubMed  Google Scholar 

    28.
    Viana, M. et al. Assembling evidence for identifying reservoirs of infection. Trends Ecol. Evol. 29, 270–279 (2014).
    PubMed  PubMed Central  Google Scholar 

    29.
    Fenton, A., Streicker, D. G., Petchey, O. L. & Pedersen, A. B. Are all hosts created equal? Partitioning host species contributions to parasite persistence in multihost communities. Am. Nat. 186, 610–622 (2015).
    PubMed  PubMed Central  Google Scholar 

    30.
    Fichet-Calvet, E. et al. Fluctuation of abundance and Lassa virus prevalence in Mastomys natalensis in Guinea, West Africa. Vector-Borne Zoonotic Dis. 7, 119–128 (2007).
    PubMed  Google Scholar 

    31.
    Marien, J. et al. Evaluation of rodent control to fight Lassa fever based on field data and mathematical modelling. Emerg. Microbes Infect. 8, 640–649 (2019).
    PubMed  PubMed Central  Google Scholar 

    32.
    Towner, J. S. et al. Marburg virus infection detected in a common african bat. PLoS ONE 2, e764 (2007).
    PubMed  PubMed Central  Google Scholar 

    33.
    Nziza, J. et al. Coronaviruses detected in bats in close contact with humans in Rwanda. EcoHealth 17, 152–159 (2020).
    PubMed  Google Scholar 

    34.
    Anthony, S. J. et al. Further evidence for bats as the evolutionary source of Middle East respiratory syndrome coronavirus. Mbio 8, e00373–17 (2017).
    CAS  PubMed  PubMed Central  Google Scholar 

    35.
    Ge, X.-Y. et al. Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature 503, 535–538 (2013).
    CAS  PubMed  PubMed Central  Google Scholar 

    36.
    Bird, B. H. & Mazet, J. A. K. Detection of emerging zoonotic pathogens: an integrated one health approach. Annu. Rev. Anim. Biosci. 6, 121–139 (2018).
    CAS  PubMed  Google Scholar 

    37.
    Goldstein, T. et al. The discovery of Bombali virus adds further support for bats as hosts of ebolaviruses. Nat. Microbiol. 3, 1084–1089 (2018).
    CAS  PubMed  PubMed Central  Google Scholar 

    38.
    Pernet, O. et al. Evidence for henipavirus spillover into human populations in Africa. Nat. Commun. 5, 5342 (2014).
    PubMed  PubMed Central  Google Scholar 

    39.
    Grard, G. et al. A novel rhabdovirus associated with acute hemorrhagic fever in Central Africa. PLoS Pathog. 8, e1002924 (2012).
    PubMed  PubMed Central  Google Scholar 

    40.
    Han, B. A. & Drake, J. M. Future directions in analytics for infectious disease intelligence. EMBO Rep. 17, 785–789 (2016).
    CAS  PubMed  PubMed Central  Google Scholar 

    41.
    Han, B. A., Schmidt, J. P., Bowden, S. E. & Drake, J. M. Rodent reservoirs of future zoonotic diseases. Proc. Natl Acad. Sci. USA 112, 7039–7044 (2015).
    CAS  PubMed  Google Scholar 

    42.
    Han, B. A. et al. Undiscovered bat hosts of filoviruses. PLoS Negl. Trop. Dis. 10, e0004815 (2016).
    PubMed  PubMed Central  Google Scholar 

    43.
    Guth, S., Visher, E., Boots, M. & Brook, C. E. Host phylogenetic distance drives trends in virus virulence and transmissibility across the animal-human interface. Philos. Trans. R. Soc. B 374, 20190296 (2019).
    Google Scholar 

    44.
    Olival, K. J. et al. Host and viral traits predict zoonotic spillover from mammals. Nature 546, 646–650 (2017).
    CAS  PubMed  PubMed Central  Google Scholar 

    45.
    Pepin, K. M., Lass, S., Pulliam, J. R. C., Read, A. F. & Lloyd-Smith, J. O. Identifying genetic markers of adaptation for surveillance of viral host jumps. Nat. Rev. Microbiol. 8, 802–813 (2010).
    CAS  PubMed  PubMed Central  Google Scholar 

    46.
    Babayan, S. A., Orton, R. J. & Streicker, D. G. Predicting reservoir hosts and arthropod vectors from evolutionary signatures in RNA virus genomes. Science 362, 577–580 (2018).
    CAS  PubMed  PubMed Central  Google Scholar 

    47.
    Bakker, K. M. et al. Fluorescent biomarkers demonstrate prospects for spreadable vaccines to control disease transmission in wild bats. Nat. Ecol. Evol. 3, 1697–1704 (2019).
    PubMed  PubMed Central  Google Scholar 

    48.
    Garnier, R., Gandon, S., Chaval, Y., Charbonnel, N. & Boulinier, T. Evidence of cross-transfer of maternal antibodies through allosuckling in a mammal: potential importance for behavioral ecology. Mamm. Biol. 78, 361–364 (2013).
    Google Scholar 

    49.
    Stading, B. et al. Protection of bats (Eptesicus fuscus) against rabies following topical or oronasal exposure to a recombinant raccoon poxvirus vaccine. PLoS Negl. Trop. Dis. 11, e0005958 (2017).
    PubMed  PubMed Central  Google Scholar 

    50.
    Schreiner, C. L., Nuismer, S. L. & Basinski, A. J. When to vaccinate a fluctuating wildlife population: is timing everything? J. Appl. Ecol. 57, 307–319 (2020).
    PubMed  Google Scholar 

    51.
    Varrelman, T. J., Basinski, A. J., Remien, C. H. & Nuismer, S. L. Transmissible vaccines in heterogeneous populations: implications for vaccine design. One Health 7, 100084 (2019).
    PubMed  PubMed Central  Google Scholar 

    52.
    Alizon, S., Hurford, A., Mideo, N. & Van Baalen, M. Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. J. Evol. Biol. 22, 245–259 (2009).
    CAS  PubMed  Google Scholar 

    53.
    Kew, O. M., Sutter, R. W., de Gourville, E. M., Dowdle, W. R. & Pallansch, M. A. Vaccine-derived polioviruses and the endgame strategy for global polio eradication. Annu. Rev. Microbiol. 59, 587–635 (2005).
    CAS  PubMed  Google Scholar 

    54.
    Bull, J. J. Evolutionary reversion of live viral vaccines: can genetic engineering subdue it? Virus Evol. 1, vev005 (2015).
    PubMed  PubMed Central  Google Scholar 

    55.
    Lauring, A. S., Jones, J. O. & Andino, R. Rationalizing the development of live attenuated virus vaccines. Nat. Biotechnol. 28, 573–579 (2010).
    CAS  PubMed  PubMed Central  Google Scholar 

    56.
    Nuismer, S. L., Basinski, A. & Bull, J. J. Evolution and containment of transmissible recombinant vector vaccines. Evol. Appl. 12, 1595–1609 (2019).
    PubMed  PubMed Central  Google Scholar 

    57.
    Kew, O. M. et al. Circulating vaccine-derived polioviruses: current state of knowledge. Bull. World Health Organ. 82, 16–23 (2004).
    PubMed  PubMed Central  Google Scholar 

    58.
    Hampson, K. et al. Estimating the global burden of endemic canine rabies. PLoS Negl. Trop. Dis. 9, e0003709 (2015).
    PubMed  PubMed Central  Google Scholar 

    59.
    Cost of the Ebola Epidemic (US Centers for Disease Control and Prevention, 2020); https://go.nature.com/38iF7cg

    60.
    Forum on Microbial Threats Learning from SARS: Preparing for the Next Disease Outbreak: Workshop Summary (National Academies Press, 2004). More

  • in

    Methane emission from high latitude lakes: methane-centric lake classification and satellite-driven annual cycle of emissions

    1.
    IPCC: Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change [eds. Pachauri, R.K & L.A. Meyer) (IPCC, 2014).
    2.
    AMAP (Arctic Monitoring and Assessment Programme). Snow, Water (Ice and Permafrost in the Arctic, AMAP, Tromsø, 2017).
    Google Scholar 

    3.
    Wik, M., Varner, R. K., Walter Anthony, K., MacIntyre, S. & Bastviken, D. Climate-sensitive northern lakes and ponds are critical components of methane release. Nat. Geosci. 9, 99–105 (2016).
    ADS  CAS  Article  Google Scholar 

    4.
    Holgerson, M. A. & Raymond, P. A. Large contribution to inland water CO2 and CH4 emissions from very small ponds. Nat. Geosci. 9, 222–226 (2016).
    ADS  CAS  Article  Google Scholar 

    5.
    Bastviken, D., Cole, J., Pace, M. & Tranvik, L. Methane emissions from lakes: Dependence of lake characteristics, two regional assessments, and a global estimate. Global Biogeochem. Cyc. 18, 1–12 (2004).
    Article  Google Scholar 

    6.
    Bastviken, D., Tranvik, L. J., Downing, J. A., Crill, P. M. & Enrich-Prast, A. Freshwater methane emissions offset the continental carbon sink. Science 331, 50–51 (2011).
    ADS  CAS  Article  Google Scholar 

    7.
    Walter, K. M., Smith, L. C. & Chapin, F. S. Methane bubbling from northern lakes: present and future contributions to the global methane budget. Philos. Trans. R. Soc. A 365, 1657–1676 (2007).
    ADS  CAS  Article  Google Scholar 

    8.
    Walter Anthony, K. M. & Anthony, P. Constraining spatial variability of methane ebullition seeps in thermokarst lakes using point process models. J. Geophys. Res. Biogeosci. 118, 1015–1034. https://doi.org/10.1002/jgrg.20087 (2013).
    Article  Google Scholar 

    9.
    Tan, Z. & Zhuang, Q. Arctic lakes are continuous methane sources to the atmosphere under warming conditions. Environ. Res. Lett. 10, 1–9 (2015).
    Article  Google Scholar 

    10.
    Tan, Z. & Zhuang, Q. Methane emissions from pan-Arctic lakes during the 21st century: An analysis with process-based models of lake evolution and biogeochemistry. J. Geophys. Res. Biogeosci. 120, 2641 (2015).
    CAS  Article  Google Scholar 

    11.
    Lehner, B. & Doell, P. Development and validation of a global database of lakes, reservoirs and wetlands. J. Hydrol. 296, 1–22 (2004).
    ADS  Article  Google Scholar 

    12.
    Verpoorter, C., Kutser, T., Seekell, D. A. & Tranvik, L. J. A global inventory of lakes based on high-resolution satellite imagery. Geophys. Res. Lett. 41, 6396–6402 (2014).
    ADS  Article  Google Scholar 

    13.
    Messager, M. L., Lehner, B., Grill, G., Nedeva, I. & Schmitt, O. Estimating the volume and age of water stored in global lakes using a geo-statistical approach. Nat. Commun. 7, 13603 (2016).
    ADS  CAS  Article  Google Scholar 

    14.
    Downing, J. A. & Duarte, C. M. Abundance and size distribution of lakes, ponds, and impoundments. In Encyclopedia of Inland Water, 1 (ed. Likens, G. E.) 469–478 (Elsevier, Amsterdam, 2009).
    Google Scholar 

    15.
    McGinnis, D. F., Greinert, J., Artemov, Y., Beaubien, S. E. & Wüest, A. Fate of rising methane bubbles in stratified waters: how much methane reaches the atmosphere?. J. Geophys. Res. 111, C09007 (2006).
    ADS  Article  Google Scholar 

    16.
    Lamarche, C. et al. Compilation and validation of SAR and optical data products for a complete and global map of inland/ocean water tailored to the climate modeling community. Rem. Sens. 9, 36 (2017).
    ADS  Article  Google Scholar 

    17.
    Pekel, J.-F., Cottam, A., Gorelick, N. & Belward, A. S. High-resolution mapping of global surface water and its long-term changes. Nature 540, 418–422 (2016).
    ADS  CAS  Article  Google Scholar 

    18.
    Sanches, L. F., Guenet, B., Marinho, C. C., Barros, N. & de Assis Esteves, F. Global regulation of methane emission from natural lakes. Sci. Rep. 9, 255 (2019).
    ADS  Article  Google Scholar 

    19.
    Bruhwiler, L. et al. CarbonTracker-CH4: an assimilation system for estimating emissions of atmospheric methane. Atmos. Chem. Phys. 14, 8269–8293 (2014).
    ADS  Article  Google Scholar 

    20.
    Du, J., Kimball, J. S., Duguay, C., Kim, Y. & Watts, J. D. Satellite microwave assessment of Northern Hemisphere lake ice phenology from 2002 to 2015. Cryosphere 11, 47–63 (2017).
    ADS  Article  Google Scholar 

    21.
    Kim, Y., Kimball, J. S., McDonald, K. C. & Glassy, J. Developing a global data record of daily landscape freeze/thaw status using satellite microwave remote sensing, Version 4. IEEE Trans. Geosci. Rem. Sens. 49, 949–960 (2016).
    ADS  Article  Google Scholar 

    22.
    Brown, J., Ferrians, O.J., Heginbottom, J.A. & Melnikov, E.S. Circum-Arctic map of permafrost and ground-ice conditions, Version 2. Boulder, CO, National Snow and Ice Data Center/World Data Center for Glaciology. https://doi.org/10.3133/cp45 (2002).

    23.
    Obu, J. et al. Northern hemisphere permafrost map based on TTOP modelling for 2000–2016 at 1 km2 scale. Earth Sci. Rev. 193, 299–316 (2019).
    ADS  Article  Google Scholar 

    24.
    Harmonized World Soil Database (HWSD) https://daac.ornl.gov/SOILS/guides/HWSD.html.

    25.
    Allen, G. H. & Pavelsky, T. M. Global extent of rivers and streams. Science 361, 585–588 (2018).
    MathSciNet  CAS  Article  Google Scholar 

    26.
    Lehner, B. et al. High-resolution mapping of the world’s reservoirs and dams for sustainable river-flow management. Front. Ecol. Environ. 9(9), 494–502 (2011).
    Article  Google Scholar 

    27.
    Mulligan, M., Saenz-Cruz, L., van Soesbergen, A., Smith, V.T. & Zurita, L. The Global georeferenced Database of Dams (GOOD2), Version 1. Global dams database and geowiki. https://geodata.policysupport.org/dams (2009).

    28.
    Chau, Y. K., Snodgrass, W. J. & Wong, P. T. S. A sampler for collecting evolved gases from sediment. Water Res. 11, 807–809 (1977).
    CAS  Article  Google Scholar 

    29.
    Howard, D.L., Frea, J.I. & Pfister, R.M. The potential for methane carbon cycling in Lake Erie. In Paper Presented at 14th Conference on Great Lakes Research (Int. Assoc. of Great Lakes Res., Ann Arbor, Mich. 1971).

    30.
    Townsend-Small, A. et al. Quantifying emissions of methane derived from anaerobic organic matter respiration and natural gas extraction in Lake Erie. Limnol. Oceanogr. 61, S356–S366 (2016).
    CAS  Article  Google Scholar 

    31.
    Joung, D., Leonte, M. & Kessler, J. D. Methane sources in the waters of Lake Michigan and Lake Superior as revealed by natural radiocarbon measurements. Geophys. Res. Lett. 46, 5436–5444 (2019).
    ADS  CAS  Article  Google Scholar 

    32.
    Shimoda, Y. et al. Our current understanding of lake ecosystem response to climate change: what have we really learned from the north temperate deep lakes?. J. Great Lakes Res. 37, 173–193 (2011).
    CAS  Article  Google Scholar 

    33.
    Blenckner, T. R. et al. Large-scale climatic signatures in lakes across Europe: a meta-analysis. Glob. Change Biol. 13, 1314–1326 (2007).
    ADS  Article  Google Scholar 

    34.
    van Huissteden, J. et al. Methane emissions from permafrost thaw lakes limited by lake drainage. Nat. Clim. Change 1, 119–123 (2011).
    ADS  Article  Google Scholar 

    35.
    Kalff, J. Limnology, Inland Water Ecosystems (Prentice Hall, Upper Saddle River, 2002).
    Google Scholar 

    36.
    Kourzeneva, E., Asensio, H., Martin, E. & Faroux, S. Global gridded dataset of lake coverage and lake depth for use in numerical weather prediction and climate modelling. Tellus A 64, 1–14 (2012).
    Google Scholar  More

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    Estimating illegal fishing from enforcement officers

    Experimental design
    Following five focus groups with SERNAPESCA’s head of enforcement and other personnel, we designed and implemented an online survey that targeted fisheries enforcement officers who are responsible for monitoring IUU activities in Chile. The survey was structured to capture expert knowledge on various aspects of illegal activities, as well as the relative experience of the officers. The survey defined illegal fishing as a fishing activity carried out in national jurisdiction waters by national or international boats that is in violation of the national fishing law, conducted without a legal permit, or activities that involve unreported or misreported captures to the authorities. The Director of SERNAPESCA delivered the survey via email to all SERNAPESCA enforcement officers. The list of officers was constructed by the Director (n = 86). The survey was anonymous in that the officers were not asked to report their name nor any information that could be used for identification (e.g., email). Answers to questions were not mandatory; that is, respondents could opt-out of answering particular questions and continue with the survey. The survey was available online for ten weeks, over which five reminder emails were sent to officers requesting them to complete the survey.
    The survey, in Spanish, consisted of two sections. First, we asked respondents to rank the magnitude of illegal activity for twenty fisheries on a nominal scale (1–5), along with their relative experience with each fishery (nominal scale, 1–5). The twenty fisheries were selected a priori based on our focus groups and known information about illegal activity. All fisheries were single species, with the exception of four that included multiple species: skates (2 species, Zearaja chilensis and Bathyraja macloviana), kelp (4 species: Lessonia spicate, L. berteroana, L. traberculata, Macrocystis pyrifera), red algae (3 species: Sarcothalia crispate, Gigartina skottsbergii, Mazzaella laminarioides), and crabs (10 species excluding southern king crab: Cancer edwardsi, C. porter, C. setosus, C. coronatus, Homalaspis plana, Ovalipes trimaculatus, Taliepus dentatus, T. marginatus, Mursia gaudichaudi, Hemigrapsus crenulatus). In the second part of the survey, we asked respondents additional questions for four focal fisheries: South Pacific hake (Merluccius gayi gayi), southern hake (M. australis), loco or Chilean abalone (Concholepas concholepas), and kelp. For each fishery, we asked respondents to score on a nominal scale (1–5),

    The frequency of six specific illegal activities in the industrial sector: size, gear, season, area, transshipment, and port.

    The frequency of six specific illegal activities in the small-scale sector: size, gear, season, area, transshipment, and port.

    The participation of illegal activity for six different stakeholders along the supply chain: fisher, purchaser, processor, wholesaler, exporter, and restaurateur.

    The utilization of seven infrastructure types in illegal activities: fishing boats, refrigeration trucks, processing plants, markets, transshipment boats, export vehicles, and restaurants.

    This study was approved by the Advanced Conservation Strategies and Pontificia Universidad Católica ethics institutional review boards and followed guidelines established by their ethics committees, which complies with national and international standards. The surveys included a written informed consent approved by all interviewees, which acknowledged research objectives and established that the survey was anonymous and that interviewees were free to choose to not answer questions. While all species have common names in Chile (which were used in the survey), we use Fishbase and Sealifebase as the taxonomic authority and for the common names reported here to facilitate comparisions34,35.
    Statistical analysis
    For both sections of the survey, we used a Bayesian cumulative multinomial logit model to predict illegal estimates. First, we fitted a model for illegal estimates for each of the twenty fisheries jointly. Second, we fitted models for illegal estimates for various aspects of the four focal fisheries (i.e., activities, stakeholders, and infrastructure) in a single analysis for each aspect. In both models, we included a random intercept term for respondent, along with a fixed effect for fishery. We evaluated the role of experience, as self-reported by the respondents, by comparing the difference between the illegal score by a respondent for a fishery and the model prediction for that fishery across respondents. If higher levels of expertise increased or decreased the value of a respondent’s scoring, there would be a relationship between the size of the differences and the level of experience reported for a fishery. Experience may also affect the difference in mean responses (i.e., bias), potentially due to more personal experience over a longer period of time, which would lead to a correlation between expertise and mean illegality scores. Depending on the patterns observed in the data, there are several ways to control for a respondent’s experience in illegality estimates. In our case, we used experience scores as a covariate in the model.
    For the twenty fisheries, we used the following model,

    $$Prleft{{S}_{ij}=kright}=phi left({tau }_{k}-left({varvec{beta}}{{varvec{x}}}_{{varvec{i}}}+{{varvec{z}}}_{{varvec{j}}}{{varvec{V}}}_{{varvec{i}}}right)right)-phi left({tau }_{k-1}-left({varvec{beta}}{{varvec{x}}}_{{varvec{i}}}+{{varvec{z}}}_{{varvec{j}}}{{varvec{V}}}_{{varvec{j}}}right)right)$$
    (1)

    in which the probability that the score for the level of illegal landings ({S}_{ij}) for the ith species by the jth respondent is equal to category k, can be represented as a latent continuous variable which is divided into K categories, by K − 1 thresholds at ({tau }_{k}). This latent continuous variable is represented by the cumulative normal distribution, (phi). For a given observation, the regression equation is composed of coefficients multiplied times predictor variables ({varvec{beta}}{{varvec{x}}}_{{varvec{i}}}) plus a design matrix for the random effect, multiplied times the error term for the jth respondent, ({{varvec{z}}}_{{varvec{j}}}{{varvec{V}}}_{{varvec{i}}}) . The probability of that observation falling in category k, (Prleft{{S}_{ij}=kright}), is thus the probability of it being in a category equal to or smaller than k, (phi left({tau }_{k}-left({varvec{beta}}{{varvec{x}}}_{{varvec{i}}}+{{varvec{z}}}_{{varvec{j}}}{{varvec{V}}}_{{varvec{i}}}right)right)), less the probability of the observation being in a category smaller than k, (phi left({tau }_{k-1}-left({varvec{beta}}{{varvec{x}}}_{{varvec{i}}}+{{varvec{z}}}_{{varvec{j}}}{{varvec{V}}}_{{varvec{j}}}right)right)). Implemented in the R statistical language, using the brms package36, the call to fit this model looks like the following:

    $${text{Score}}; , sim ;{text{Species}} + {text{Experience }} + left( {{1}|{text{Respondent}}} right),;{text{ data}} = {text{SurveyData}},;{text{family}} = {text{cumulative}}),$$

    where Score is ({S}_{ij}) in (1) above, the fixed effects, ({varvec{beta}}{{varvec{x}}}_{{varvec{i}}}) are the experience of the respondent and the species that was scored, and (1|Respondent) denotes a random intercept model, where each has a different intercept term, drawn from a shared error distribution. For more information on the application of this model to ordinal response data, see Burkner and Vuorre37.
    For the estimates for the various aspects of the four focal fisheries, we used the following model,

    $${text{Response}}; sim ;{text{Species}} + {text{Experience}} + left( {{1}|{text{Respondent}}} right),;{text{data}} = {text{SurveyData}},;{text{family}} = {text{cumulative}}),$$

    which is structured as per (1) above, but with the responses to the various focal species questions (i.e., activities per sector, stakeholders, and infrastructure) substituted for the species scores as in (1).
    We compared both models with simpler models, including a single-term null model using leave-one-out cross-validation. We did so in the R statistical language using the loo packages36,38,39. Prior distributions for all regression terms were improper flat priors over the real numbers, the default in the brms package for population parameters. The priors on the intercept and the random effects were student t3,0,10 distributions, as per the default for uninformative priors in the brms package.
    We carried out a Principal Components Analysis (PCA) with the four focal fisheries as categorical variables and the illegal activity, stakeholder, and infrastructure estimates from the Bayesian cumulative multinomial logit model. For each fishery, we used 10,000 estimates from the model, along with a qualitative variable that represented the different factors (e.g., restaurateur). The latter has no influence on the principal components of the analysis but helps to interpret the dimensions of variability. Principal Components Analysis is especially powerful as an approach to visualize patterns, such as clusters, clines, and outliers in a dataset40. In our case, we sought to visualize whether there were common illegal factors with similar set of scores and whether there was any association between high or low scores of illegal factors and the focal fisheries. We used the FactoMineR package in the R statistical language41. More

  • in

    Glycan degradation writ large in the ocean

    1.
    Sichert, A. et al. Nat. Microbiol. https://doi.org/10.1038/s41564-020-0720-2 (2020).
    Article  PubMed  Google Scholar 
    2.
    Krause-Jensen, D. & Duarte, C. Nat. Geosci. 9, 737–742 (2016).
    CAS  Article  Google Scholar 

    3.
    Wang, M. et al. Science 365, 83–87 (2019).
    CAS  Article  Google Scholar 

    4.
    Sakai, T., Ishizuka, K. & Kato, I. Mar. Biotechnol. 5, 409–416 (2003).
    CAS  Article  Google Scholar 

    5.
    Ndeh, D. et al. Nature 544, 65–70 (2017).
    CAS  Article  Google Scholar 

    6.
    Rogowski, A. et al. Nat. Commun. 6, 7481 (2015).
    CAS  Article  Google Scholar 

    7.
    Petit, E. et al. PLoS ONE 8, e54337 (2013).
    CAS  Article  Google Scholar 

    8.
    Desai, M. S. et al. Cell 167, 1339–1353 (2016).
    CAS  Article  Google Scholar 

    9.
    Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P. M. & Henrissat, B. Nucleic Acids Res. 42, D490–D495 (2014).
    CAS  Article  Google Scholar  More

  • in

    Rhizobiome shields plants from infection

    1.
    Toruño, T. Y., Stergiopoulos, I. & Coaker, G. Annu. Rev. Phytopathol. 54, 419–441 (2016).
    Article  Google Scholar 
    2.
    Elphinstone, J. in Bacterial Wilt Disease and the Ralstonia solanacearum Complex (eds Allen, C. et al.) 9–28 (APS Press, 2005).

    3.
    Gu, S. et al. Nat. Microbiol. https://doi.org/10.1038/s41564-020-0719-8 (2020).

    4.
    Bossier, P., Hofte, M. & Verstraete, W. in Advances in Microbial Ecology (ed. Marshall, K. C.) 385–414 (Springer, 1988).

    5.
    Miethke, M. & Marahiel, M. A. Microbiol. Mol. Biol. Rev. 71, 413–451 (2007).
    CAS  Article  Google Scholar 

    6.
    Winkelmann, G. in Iron Transport in Bacteria (eds Crosa, J. H. et al.) 435–450 (John Wiley & Sons, 2014).

    7.
    Lee, W., van Baalen, M. & Jansen, V. A. A. Ecol. Lett. 15, 119–125 (2012).
    Article  Google Scholar  More

  • in

    Termite mounds contain soil-derived methanotroph communities kinetically adapted to elevated methane concentrations

    1.
    Brune A. Methanogenesis in the digestive tracts of insects. In: Timmis KN (ed). Handbook of hydrocarbon and lipid microbiology. Berlin, Heidelberg: Springer-Verlag; 2010. pp. 707–728.
    2.
    Zimmerman PR, Greenberg JP, Wandiga SO, Crutzen PJ. Termites: a potentially large source of atmospheric methane, carbon dioxide, and molecular hydrogen. Science. 1982;218:563–5.
    CAS  PubMed  Google Scholar 

    3.
    Rasmussen RA, Khalil MAK. Global production of methane by termites. Nature. 1983;301:700.
    CAS  Google Scholar 

    4.
    Sugimoto A, Inoue T, Tayasu I, Miller L, Takeichi S, Abe T. Methane and hydrogen production in a termite-symbiont system. Ecol Res. 1998;13:241–57.
    CAS  Google Scholar 

    5.
    Brauman A, Kane MD, Labat M, Breznak JA. Genesis of acetate and methane by gut bacteria of nutritionally diverse termites. Science. 1992;257:1384–7.
    CAS  PubMed  Google Scholar 

    6.
    Kirschke S, Bousquet P, Ciais P, Saunois M, Canadell JG, Dlugokencky EJ, et al. Three decades of global methane sources and sinks. Nat Geosci. 2013;6:813–23.
    CAS  Google Scholar 

    7.
    Nauer PA, Hutley LB, Arndt SK. Termite mounds mitigate half of termite methane emissions. Proc Natl Acad Sci USA. 2018;115:13306–11.
    CAS  PubMed  Google Scholar 

    8.
    Hanson RS, Hanson TE. Methanotrophic bacteria. Microbiol Rev. 1996;60:439–71.
    CAS  PubMed  PubMed Central  Google Scholar 

    9.
    Reuß J, Rachel R, Kämpfer P, Rabenstein A, Küver J, Dröge S, et al. Isolation of methanotrophic bacteria from termite gut. Microbiol Res. 2015;179:29–37.
    PubMed  Google Scholar 

    10.
    Pester M, Tholen A, Friedrich MW, Brune A. Methane oxidation in termite hindguts: absence of evidence and evidence of absence. Appl Environ Microbiol. 2007;73:2024–8.
    CAS  PubMed  PubMed Central  Google Scholar 

    11.
    Dunfield PF. The soil methane sink. In: Reay D, Hewitt K, Smith K, Grace J, editors. Greenhouse gas sinks. Wallingford: CABI; 2007. pp. 152–70.

    12.
    Bignell DE, Eggleton P, Nunes L, Thomas KL. Termites as mediators of forest carbon fluxes in tropical forests: budgets for carbon dioxide and methane emissions. In: Watt AD, Stork NE, Hunter MD (eds). Forests and insects. London: Chapman & Hall; 1997. pp. 109–134.

    13.
    Jamali H, Livesley SJ, Grover SP, Dawes TZ, Hutley LB, Cook GD, et al. The importance of termites to the CH4 balance of a tropical savanna woodland of northern Australia. Ecosystems. 2011;14:698–709.
    CAS  Google Scholar 

    14.
    Ho A, Erens H, Mujinya BB, Boeckx P, Baert G, Schneider B, et al. Termites facilitate methane oxidation and shape the methanotrophic community. Appl Environ Microbiol. 2013;79:7234–40.
    CAS  PubMed  PubMed Central  Google Scholar 

    15.
    Noirot C, Darlington JPEC. Termite nests: architecture, regulation and defence. In: Abe T, Bignell DE, Higashi M (eds). Termites: Evolution, Sociality Symbioses, Ecology. Dordrecht: Springer; 2000. pp. 121–139.

    16.
    Korb J. Termite mound architecture, from function to construction. In: Bignell DE, Roisin Y, Lo N (eds). Biology of termites: a modern synthesis. Dordrecht: Springer Netherlands; 2010. pp. 349–373.

    17.
    Jones DT, Eggleton P. Global biogeography of termites: a compilation of sources. In: Bignell DE, Roisin Y, Lo N, editors. Biology of termites: a modern synthesis. Dordrecht: Springer; 2011. pp. 1–576.

    18.
    Knief C. Diversity and habitat preferences of cultivated and uncultivated aerobic methanotrophic bacteria evaluated based on pmoA as molecular marker. Front Microbiol. 2015;6:1346.
    PubMed  PubMed Central  Google Scholar 

    19.
    Nauer PA, Chiri E, Souza D, de, Hutley LB, Arndt SK. Rapid image-based field methods improve the quantification of termite mound structures and greenhouse-gas fluxes. Biogeosciences. 2018;15:3731–42.
    Google Scholar 

    20.
    Holmes AJ, Costello A, Lidstrom ME, Murrell JC. Evidence that participate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. FEMS Microbiol Lett. 1995;132:203–8.
    CAS  PubMed  PubMed Central  Google Scholar 

    21.
    Costello AM, Lidstrom ME. Molecular characterization of functional and phylogenetic genes from natural populations of methanotrophs in lake sediments. Appl Environ Microbiol. 1999;65:5066–74.
    CAS  PubMed  PubMed Central  Google Scholar 

    22.
    Henneberger R, Chiri E, Bodelier PEL, Frenzel P, Lüke C, Schroth MH. Field‐scale tracking of active methane‐oxidizing communities in a landfill cover soil reveals spatial and seasonal variability. Environ Microbiol. 2015;17:1721–37.
    CAS  PubMed  Google Scholar 

    23.
    Ji R, Brune A. Nitrogen mineralization, ammonia accumulation, and emission of gaseous NH3 by soil-feeding termites. Biogeochemistry. 2006;78:267–83.
    Google Scholar 

    24.
    Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA. 2011;108:4516–22.
    CAS  PubMed  Google Scholar 

    25.
    Parada AE, Needham DM, Fuhrman JA. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol. 2016;18:1403–14.
    CAS  PubMed  Google Scholar 

    26.
    Apprill A, McNally S, Parsons R, Weber L. Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquat Micro Ecol. 2015;75:129–37.
    Google Scholar 

    27.
    Heil JR, Lynch MDJ, Cheng J, Matysiakiewicz O, D’Alessio M, Charles TC. The completed PacBio single-molecule real-time sequence of Methylosinus trichosporium strain OB3b reveals the presence of a third large plasmid. Genome Announc. 2017;5:e01349–17.
    PubMed  PubMed Central  Google Scholar 

    28.
    Kolb S, Knief C, Stubner S, Conrad R. Quantitative detection of methanotrophs in soil by novel pmoA-targeted real-time PCR assays. Appl Environ Microbiol. 2003;69:2423–9.
    CAS  PubMed  PubMed Central  Google Scholar 

    29.
    Kolb S, Knief C, Dunfield PF, Conrad R. Abundance and activity of uncultured methanotrophic bacteria involved in the consumption of atmospheric methane in two forest soils. Environ Microbiol. 2005;7:1150–61.
    CAS  PubMed  Google Scholar 

    30.
    Větrovský T, Baldrian P. The variability of the 16S rRNA gene in bacterial genomes and its consequences for bacterial community analyses. PLoS ONE. 2013;8:e57923.
    PubMed  PubMed Central  Google Scholar 

    31.
    Chiri E, Nauer PA, Rainer E-M, Zeyer J, Schroth MH. High temporal and spatial variability of atmospheric-methane oxidation in Alpine glacier-forefield soils. Appl Environ Microbiol. 2017;83:e01139–17.
    CAS  PubMed  PubMed Central  Google Scholar 

    32.
    Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460–1.
    CAS  PubMed  Google Scholar 

    33.
    Wen X, Yang S, Liebner S. Evaluation and update of cutoff values for methanotrophic pmoA gene sequences. Arch Microbiol. 2016;198:629–36.
    CAS  PubMed  Google Scholar 

    34.
    Dumont MG, Lüke C, Deng Y, Frenzel P. Classification of pmoA amplicon pyrosequences using BLAST and the lowest common ancestor method in MEGAN. Front Microbiol. 2014;5:34.
    PubMed Central  Google Scholar 

    35.
    Gouy M, Guindon S, Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol. 2010;27:221–4.
    CAS  PubMed  Google Scholar 

    36.
    Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37:852–7.
    CAS  PubMed  PubMed Central  Google Scholar 

    37.
    McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. 2013;8:e61217.
    CAS  PubMed  PubMed Central  Google Scholar 

    38.
    Rognes T, Flouri T, Nichols B, Quince C, Mahé F. VSEARCH: a versatile open source tool for metagenomics. PeerJ. 2016;4:2584.
    Google Scholar 

    39.
    Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R. UniFrac: an effective distance metric for microbial community comparison. ISME J. 2011;5:169.
    PubMed  Google Scholar 

    40.
    Andrews S. FastQC: a quality control tool for high throughput sequence data. Babraham Bioinformatics, Cambridge, UK: The Babraham Institute; 2010.

    41.
    Ewels P, Magnusson M, Lundin S, Käller M. MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics. 2016;32:3047–8.
    CAS  PubMed  PubMed Central  Google Scholar 

    42.
    Bushnell B. BBMap: A fast, accurate, splice-aware aligner. Berkeley, CA, US: Lawrence Berkeley National Lab (LBNL); 2015.

    43.
    Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2014;12:59.
    PubMed  Google Scholar 

    44.
    Nurk S, Meleshko D, Korobeynikov A, Pevzner PA. metaSPAdes: a new versatile metagenomic assembler. Genome Res. 2017;27:824–34.
    CAS  PubMed  PubMed Central  Google Scholar 

    45.
    Kang D, Li F, Kirton ES, Thomas A, Egan RS, An H, et al. MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies. PeerJ. 2019;7:e7359.
    PubMed  PubMed Central  Google Scholar 

    46.
    Wu Y-W, Tang Y-H, Tringe SG, Simmons BA, Singer SW. MaxBin: an automated binning method to recover individual genomes from metagenomes using an expectation-maximization algorithm. Microbiome. 2014;2:26.
    CAS  PubMed  PubMed Central  Google Scholar 

    47.
    Alneberg J, Bjarnason BS, De Bruijn I, Schirmer M, Quick J, Ijaz UZ, et al. Binning metagenomic contigs by coverage and composition. Nat Methods. 2014;11:1144.
    CAS  PubMed  Google Scholar 

    48.
    Sieber CMK, Probst AJ, Sharrar A, Thomas BC, Hess M, Tringe SG, et al. Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy. Nat Microbiol. 2018;3:836–43.

    49.
    Laczny CC, Sternal T, Plugaru V, Gawron P, Atashpendar A, Margossian HH, et al. VizBin—an application for reference-independent visualization and human-augmented binning of metagenomic data. Microbiome. 2015;3:1–7.
    PubMed  PubMed Central  Google Scholar 

    50.
    Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25:1043–55.
    CAS  PubMed  PubMed Central  Google Scholar 

    51.
    Olm MR, Brown CT, Brooks B, Banfield JF. dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication. ISME J. 2017;11:2864.
    CAS  PubMed  PubMed Central  Google Scholar 

    52.
    Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A, Chaumeil P-A, et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol. 2018;36:996–1004.
    CAS  Google Scholar 

    53.
    Rusley C, Onstott TC, Vishnivetskaya TA, Layton A, Chauhan A, Pfiffner SM, et al. Metagenome-assembled genome of USCα AHI, a potential high-affinity methanotroph from Axel Heiberg Island, Canadian High Arctic. Microbiol Resour Announc. 2019;8:1–4.
    Google Scholar 

    54.
    Ricke P, Kube M, Nakagawa S, Erkel C, Reinhardt R, Liesack W. First genome data from uncultured upland soil cluster alpha methanotrophs provide further evidence for a close phylogenetic relationship to Methylocapsa acidiphila. Appl Environ Microbiol. 2005;71:7472–82.
    CAS  PubMed  PubMed Central  Google Scholar 

    55.
    Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2014;32:268–74.
    PubMed  PubMed Central  Google Scholar 

    56.
    Le SQ, Gascuel O. An improved general amino acid replacement matrix. Mol Biol Evol. 2008;25:1307–20.
    CAS  PubMed  Google Scholar 

    57.
    Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 2019;47:W256–9.
    CAS  PubMed  PubMed Central  Google Scholar 

    58.
    Dong X, Strous M. An integrated pipeline for annotation and visualization of metagenomic contigs. Front Genet. 2019;10:1–10.
    Google Scholar 

    59.
    Zhou Z, Tran P, Liu Y, Kieft K, Anantharaman K. METABOLIC: a scalable high-throughput metabolic and biogeochemical functional trait profiler based on microbial genomes. bioRxiv. 2019:761643.

    60.
    Urmann K, Gonzalez-Gil G, Schroth MH, Hofer M, Zeyer J. New field method: gas push–pull test for the in-situ quantification of microbial activities in the vadose zone. Environ Sci Technol. 2005;39:304–10.
    CAS  PubMed  Google Scholar 

    61.
    Reim A, Lüke C, Krause S, Pratscher J, Frenzel P. One millimetre makes the difference: high-resolution analysis of methane-oxidizing bacteria and their specific activity at the oxic–anoxic interface in a flooded paddy soil. ISME J. 2012;6:2128.
    CAS  PubMed  PubMed Central  Google Scholar 

    62.
    Raj SS, Sumangala RK, Lal KB, Panicker PK. Gas chromatographic analysis of oxygen and argon at room temperature. J Chromatogr Sci. 1996;34:465–7.
    Google Scholar 

    63.
    Schroth MH, Istok JD. Models to determine first‐order rate coefficients from single‐well push‐pull tests. Groundwater. 2006;44:275–83.
    CAS  Google Scholar 

    64.
    Urmann K, Schroth MH, Noll M, Gonzalez‐Gil G, Zeyer J. Assessment of microbial methane oxidation above a petroleum‐contaminated aquifer using a combination of in situ techniques. J Geophys Res Biogeosciences. 2008;113:G02006.

    65.
    R Development Core Team. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2017.
    Google Scholar 

    66.
    Holt JA. Microbial activity in the mounds of some Australian termites. Appl Soil Ecol. 1998;9:183–7.
    Google Scholar 

    67.
    Knief C, Lipski A, Dunfield PF. Diversity and activity of methanotrophic bacteria in different upland soils. Appl Environ Microbiol. 2003;69:6703–14.
    CAS  PubMed  PubMed Central  Google Scholar 

    68.
    King H, Ocko S, Mahadevan L. Termite mounds harness diurnal temperature oscillations for ventilation. Proc Natl Acad Sci USA. 2015;112:11589–93.
    CAS  PubMed  Google Scholar 

    69.
    Bristow KL, Holt JA. Can termites create local energy sinks to regulate mound temperature? J Therm Biol. 1987;12:19–21.
    Google Scholar 

    70.
    Tveit AT, Hestnes AG, Robinson SL, Schintlmeister A, Dedysh SN, Jehmlich N, et al. Widespread soil bacterium that oxidizes atmospheric methane. Proc Natl Acad Sci USA. 2019;116:8515–24.
    CAS  PubMed  Google Scholar 

    71.
    Pratscher J, Vollmers J, Wiegand S, Dumont MG, Kaster A-K. Unravelling the identity, metabolic potential and global biogeography of the atmospheric methane-oxidizing upland soil cluster α. Environ Microbiol. 2018;20:1016–29.
    CAS  PubMed  PubMed Central  Google Scholar 

    72.
    Bender M, Conrad R. Kinetics of CH4 oxidation in oxic soils exposed to ambient air or high CH4 mixing ratios. FEMS Microbiol Lett. 1992;101:261–70.
    CAS  Google Scholar 

    73.
    Nauer PA, Schroth MH. In situ quantification of atmospheric methane oxidation in near-surface soils. Vadose Zo J. 2010;9:1052–62.
    CAS  Google Scholar 

    74.
    Judd CR, Koyama A, Simmons MP, Brewer P, von Fischer JC. Co-variation in methanotroph community composition and activity in three temperate grassland soils. Soil Biol Biochem. 2016;95:78–86.
    CAS  Google Scholar 

    75.
    Schroth MH, Eugster W, Gómez KE, Gonzalez-Gil G, Niklaus PA, Oester P. Above-and below-ground methane fluxes and methanotrophic activity in a landfill-cover soil. Waste Manag. 2012;32:879–89.
    CAS  PubMed  Google Scholar 

    76.
    Baani M, Liesack W. Two isozymes of particulate methane monooxygenase with different methane oxidation kinetics are found in Methylocystis sp. strain SC2. Proc Natl Acad Sci USA. 2008;105:10203–8.
    CAS  PubMed  Google Scholar 

    77.
    Gebert J, Stralis‐Pavese N, Alawi M, Bodrossy L. Analysis of methanotrophic communities in landfill biofilters using diagnostic microarray. Environ Microbiol. 2008;10:1175–88.
    CAS  PubMed  Google Scholar 

    78.
    Bowers RM, Kyrpides NC, Stepanauskas R, Harmon-Smith M, Doud D, Reddy TBK, et al. Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea. Nat Biotechnol. 2017;35:725–31.
    CAS  PubMed  PubMed Central  Google Scholar 

    79.
    Ji M, Greening C, Vanwonterghem I, Carere CR, Bay SK, Steen JA, et al. Atmospheric trace gases support primary production in Antarctic desert surface soil. Nature. 2017;552:400–3.
    CAS  PubMed  Google Scholar 

    80.
    Pratscher J, Dumont MG, Conrad R. Assimilation of acetate by the putative atmospheric methane oxidizers belonging to the USCα clade. Environ Microbiol. 2011;13:2692–701.
    CAS  PubMed  Google Scholar 

    81.
    Greening C, Biswas A, Carere CR, Jackson CJ, Taylor MC, Stott MB, et al. Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival. ISME J. 2016;10:761–77.
    CAS  PubMed  Google Scholar 

    82.
    Cordero PRF, Bayly K, Leung PM, Huang C, Islam ZF, Schittenhelm RB, et al. Atmospheric carbon monoxide oxidation is a widespread mechanism supporting microbial survival. ISME J. 2019;13:2868–81.
    CAS  PubMed  PubMed Central  Google Scholar 

    83.
    Carere CR, Hards K, Houghton KM, Power JF, McDonald B, Collet C, et al. Mixotrophy drives niche expansion of verrucomicrobial methanotrophs. ISME J. 2017;11:2599–610.
    PubMed  PubMed Central  Google Scholar 

    84.
    Schmitz RA, Pol A, Mohammadi SS, Hogendoorn C, van Gelder AH, Jetten MSM, et al. The thermoacidophilic methanotroph Methylacidiphilum fumariolicum SolV oxidizes subatmospheric H2 with a high-affinity, membrane-associated [NiFe] hydrogenase. ISME J. 2020;14:1223.

    85.
    Mohammadi SS, Pol A, van Alen T, Jetten MSM, Op, den Camp HJM. Ammonia oxidation and nitrite reduction in the verrucomicrobial methanotroph Methylacidiphilum fumariolicum SolV. Front Microbiol. 2017;8:1901.
    PubMed  PubMed Central  Google Scholar 

    86.
    Jamali H, Livesley SJ, Hutley LB, Fest B, Arndt SK. The relationships between termite mound CH4/CO2 emissions and internal concentration ratios are species specific. Biogeosciences. 2013;10:2229–40.
    CAS  Google Scholar 

    87.
    Schnell S, King GM. Mechanistic analysis of ammonium inhibition of atmospheric methane consumption in forest soils. Appl Environ Microbiol. 1994;60:3514–21.
    CAS  PubMed  PubMed Central  Google Scholar 

    88.
    Carlsen HN, Joergensen L, Degn H. Inhibition by ammonia of methane utilization in Methylococcus capsulatus (Bath). Appl Microbiol Biotechnol. 1991;35:124–7.
    CAS  Google Scholar 

    89.
    Bodelier PLE, Laanbroek HJ. Nitrogen as a regulatory factor of methane oxidation in soils and sediments. Fems Microbiol Ecol. 2004;47:265–77.
    CAS  PubMed  Google Scholar 

    90.
    Veraart AJ, Steenbergh AK, Ho A, Kim SY, Bodelier PLE. Beyond nitrogen: the importance of phosphorus for CH4 oxidation in soils and sediments. Geoderma. 2015:259–60.

    91.
    Chiri E, Nauer PA, Henneberger R, Zeyer J, Schroth MH. Soil–methane sink increases with soil age in forefields of Alpine glaciers. Soil Biol Biochem. 2015;84:83–95.
    CAS  Google Scholar 

    92.
    Angel R, Conrad R. In situ measurement of methane fluxes and analysis of transcribed particulate methane monooxygenase in desert soils. Environ Microbiol. 2009;11:2598–610.
    CAS  PubMed  Google Scholar 

    93.
    de Caritat P, Cooper M, Wilford J. The pH of Australian soils: field results from a national survey. Soil Res. 2011;49:173–82.
    Google Scholar  More

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    Recreating Wakanda by promoting Black excellence in ecology and evolution

    To authentically be a welcoming space for Black scholars, we need to accept the full expression of Black excellence in all its forms. Concurrently, that means interrogating how societal norms and stereotypes coerce Black scientists to conform or assimilate to a strict definition of professionalism6. We do not accept species uniformity in promoting healthy ecosystems, so why would we expect assimilation of personalities, values and cultures? Recent social media movements, including but not limited to #BlackBirdersWeek, #BlackintheIvory and #BlackinNature, illustrate the myriad forms of Black scholarship, education and outreach5. Undervaluing these stories, narratives and identities negates the positive contributions our non-Black colleagues make in fighting structural racism.
    Support and fight alongside your Black colleagues against racial oppression, especially when it is inconvenient and outside our academic walls. This is especially pertinent for field biologists, as our right to belong in nature without fear of persecution or violence is under constant threat25,26. The compounding and pervasive impacts of environmental racism in conservation and environmental movements all contribute to marginalizing Black scholars’ contributions to field ecology and biology16,25,26. Authentically recognizing Black excellence will likely mean confronting authority figures (that is, police, deans, chancellors, society presidents, department chairs and so on) and using your privilege to protect the rights of your colleagues. More

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    The potential for a CRISPR gene drive to eradicate or suppress globally invasive social wasps

    1.
    Teem, J. L. et al. Genetic biocontrol for invasive species. Front. Bioeng. Biotechnol. 8, 452. https://doi.org/10.3389/fbioe.2020.00452 (2020).
    Article  PubMed  PubMed Central  Google Scholar 
    2.
    McFarlane, G. R., Whitelaw, C. B. A. & Lillico, S. G. CRISPR-based gene drives for pest control. Trends Biotechnol. 36, 130–133. https://doi.org/10.1016/j.tibtech.2017.10.001 (2018).
    CAS  Article  PubMed  Google Scholar 

    3.
    Dearden, P. K. et al. The potential for the use of gene drives for pest control in New Zealand: a perspective. J. R. Soc. N. Z. 48, 225–244. https://doi.org/10.1080/03036758.2017.1385030 (2017).
    Article  Google Scholar 

    4.
    Esvelt, K. M., Smidler, A. L., Catteruccia, F. & Church, G. M. Concerning RNA-guided gene drives for the alteration of wild populations. eLife 3, e03401. https://doi.org/10.7554/eLife.03401 (2014).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    5.
    Barrangou, R. & Doudna, J. A. Applications of CRISPR technologies in research and beyond. Nat. Biotechnol. 34, 933–941. https://doi.org/10.1038/nbt.3659 (2016).
    CAS  Article  PubMed  Google Scholar 

    6.
    Kandul, N. P. et al. Transforming insect population control with precision guided sterile males with demonstration in flies. Nat. Commun. 10, 84. https://doi.org/10.1038/s41467-018-07964-7 (2019).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    7.
    Kyrou, K. et al. A CRISPR-Cas9 gene drive targeting doublesex causes complete population suppression in caged Anopheles gambiae mosquitoes. Nat. Biotechnol. 36, 1062–1066. https://doi.org/10.1038/nbt.4245 (2018).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    8.
    Drury, D. W., Dapper, A. L., Siniard, D. J., Zentner, G. E. & Wade, M. J. CRISPR/Cas9 gene drives in genetically variable and nonrandomly mating wild populations. Sci. Adv. 3, e1601910. https://doi.org/10.1126/sciadv.1601910 (2017).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    9.
    Hammond, A. M. et al. The creation and selection of mutations resistant to a gene drive over multiple generations in the malaria mosquito. PLoS Genet. 13, e1007039. https://doi.org/10.1371/journal.pgen.1007039 (2017).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    10.
    Webber, B. L., Raghu, S. & Edwards, O. R. Opinion: is CRISPR-based gene drive a biocontrol silver bullet or global conservation threat?. Proc. Natl. Acad. Sci. U.S.A. 112, 10565–10567. https://doi.org/10.1073/pnas.1514258112 (2015).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    11.
    Wilkins, K. E., Prowse, T. A. A., Cassey, P., Thomas, P. Q. & Ross, J. V. Pest demography critically determines the viability of synthetic gene drives for population control. Math. Biosci. 305, 160–169. https://doi.org/10.1016/j.mbs.2018.09.005 (2018).
    MathSciNet  Article  PubMed  MATH  Google Scholar 

    12.
    de la Filia, A. G., Bain, S. A. & Ross, L. Haplodiploidy and the reproductive ecology of Arthropods. Curr. Opin. Insect Sci. 9, 36–43. https://doi.org/10.1016/j.cois.2015.04.018 (2015).
    Article  Google Scholar 

    13.
    Deredec, A., Burt, A. & Godfray, H. C. The population genetics of using homing endonuclease genes in vector and pest management. Genetics 179, 2013–2026. https://doi.org/10.1534/genetics.108.089037 (2008).
    Article  PubMed  PubMed Central  Google Scholar 

    14.
    Rode, N. O., Estoup, A., Bourguet, D., Courtier-Orgogozo, V. & Débarre, F. Population management using gene drive: molecular design, models of spread dynamics and assessment of ecological risks. Conserv. Genet. 20, 671–690. https://doi.org/10.1007/s10592-019-01165-5 (2019).
    CAS  Article  Google Scholar 

    15.
    Alphey, N. & Bonsall, M. B. Interplay of population genetics and dynamics in the genetic control of mosquitoes. J. R. Soc. Interface 11, 20131071. https://doi.org/10.1098/rsif.2013.1071 (2014).
    Article  PubMed  PubMed Central  Google Scholar 

    16.
    Prowse, T. A. A. et al. Dodging silver bullets: good CRISPR gene-drive design is critical for eradicating exotic vertebrates. Proc. R. Soc. B https://doi.org/10.1098/rspb.2017.0799 (2017).
    Article  PubMed  Google Scholar 

    17.
    Lowe, S., Browne, M., Boudjelas, S. & De Poorter, M. 100 of the World’s Worst Invasive Alien Species. A Selection from the Global Invasive Species Database Vol. 12 (The Invasive Species Specialist Group (ISSG) a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN), Auckland, 2000).
    Google Scholar 

    18.
    Lester, P. J. & Beggs, J. R. Invasion success and management strategies for social Vespula wasps. Annu. Rev. Entomol. 64, 51–71. https://doi.org/10.1146/annurev-ento-011118-111812 (2019).
    CAS  Article  PubMed  Google Scholar 

    19.
    Lester, P. J. et al. Determining the origin of invasions and demonstrating a lack of enemy release from microsporidian pathogens in common wasps (Vespula vulgaris). Divers. Distrib. 20, 964–974. https://doi.org/10.1111/ddi.12223 (2014).
    Article  Google Scholar 

    20.
    Harris, R. J. Diet of the wasps Vespula vulgaris and V. germanica in honeydew beech forest of the South Island, New Zealand. N. Z. J. Zool. 18, 159–169 (1991).
    Article  Google Scholar 

    21.
    Grangier, J. & Lester, P. J. A novel interference behaviour: invasive wasps remove ants from resources and drop them from a height. Biol. Lett. 7, 664–667. https://doi.org/10.1098/rsbl.2011.0165 (2011).
    Article  PubMed  PubMed Central  Google Scholar 

    22.
    Wilson, P. R., Karl, B. J., Toft, R. J., Beggs, J. R. & Taylor, R. H. The role of introduced predators and competitors in the decline of kaka (Nestor meridionalis) populations in New Zealand. Biol. Conserv. 83, 175–185. https://doi.org/10.1016/S0006-3207(97)00055-4 (1998).
    Article  Google Scholar 

    23.
    Dobelmann, J. et al. Fitness in invasive social wasps: the role of variation in viral load, immune response and paternity in predicting nest size and reproductive output. Oikos 126, 1208–1218. https://doi.org/10.1111/oik.04117 (2017).
    CAS  Article  Google Scholar 

    24.
    Sekine, K., Furusawa, T. & Hatakeyama, M. The boule gene is essential for spermatogenesis of haploid insect male. Dev. Biol. 399, 154–163. https://doi.org/10.1016/j.ydbio.2014.12.027 (2015).
    CAS  Article  PubMed  Google Scholar 

    25.
    Ferree, P. M. et al. Identification of genes uniquely expressed in the germ-line tissues of the jewel wasp Nasonia vitripennis. G3-Genes Genom. Genet. 5, 2647–2653. https://doi.org/10.1534/g3.115.021386 (2015).
    CAS  Article  Google Scholar 

    26.
    Mikhaylova, L. M., Boutanaev, A. M. & Nurminsky, D. I. Transcriptional regulation by Modulo integrates meiosis and spermatid differentiation in male germ line. Proc. Natl. Acad. Sci. U.S.A. 103, 11975–11980. https://doi.org/10.1073/pnas.0605087103 (2006).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    27.
    Parsch, J., Meiklejohn, C. D., Hauschteck-Jungen, E., Hunziker, P. & Hartl, D. L. Molecular evolution of the ocnus and janus genes in the Drosophila melanogaster species subgroup. Mol. Biol. Evol. 18, 801–811. https://doi.org/10.1093/oxfordjournals.molbev.a003862 (2001).
    CAS  Article  PubMed  Google Scholar 

    28.
    Dang, Y. et al. Optimizing sgRNA structure to improve CRISPR-Cas9 knockout efficiency. Genome Biol. 16, 280. https://doi.org/10.1186/s13059-015-0846-3 (2015).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    29.
    Yarrington, R. M., Verma, S., Schwartz, S., Trautman, J. K. & Carroll, D. Nucleosomes inhibit target cleavage by CRISPR-Cas9 in vivo. Proc. Natl. Acad. Sci. U.S.A. 115, 9351–9358. https://doi.org/10.1073/pnas.1810062115 (2018).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    30.
    Chaverra-Rodriguez, D. et al. Targeted delivery of CRISPR-Cas9 ribonucleoprotein into arthropod ovaries for heritable germline gene editing. Nat. Commun. 9, 3008. https://doi.org/10.1038/s41467-018-05425-9 (2018).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    31.
    Noble, C. et al. Daisy-chain gene drives for the alteration of local populations. Proc. Natl. Acad. Sci. U.S.A. 116, 8275–8282. https://doi.org/10.1073/pnas.1716358116 (2019).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    32.
    KaramiNejadRanjbar, M. et al. Consequences of resistance evolution in a Cas9-based sex conversion-suppression gene drive for insect pest management. Proc. Natl. Acad. Sci. U.S.A. 115, 6189–6194. https://doi.org/10.1073/pnas.1713825115 (2018).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    33.
    Brenton-Rule, E. C. et al. The origins of global invasions of the German wasp (Vespula germanica) and its infection with four honey bee viruses. Biol. Invasions 20, 3445–3460. https://doi.org/10.1007/s10530-018-1786-0 (2018).
    Article  Google Scholar 

    34.
    Schmack, J. M. et al. Lack of genetic structuring, low effective population sizes and major bottlenecks characterise common and German wasps in New Zealand. Biol. Invasions 21, 3185–3201. https://doi.org/10.1007/s10530-019-02039-0 (2019).
    Article  Google Scholar 

    35.
    Tanaka, H., Stone, H. A. & Nelson, D. R. Spatial gene drives and pushed genetic waves. Proc. Natl. Acad. Sci. U.S.A. 114, 8452–8457. https://doi.org/10.1073/pnas.1705868114 (2017).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    36.
    Hammond, A. et al. A CRISPR-Cas9 gene drive system targeting female reproduction in the malaria mosquito vector Anopheles gambiae. Nat. Biotechnol. 34, 78–83. https://doi.org/10.1038/nbt.3439 (2016).
    CAS  Article  PubMed  Google Scholar 

    37.
    Marshall, J. M., Buchman, A., Sanchez, C. H. & Akbari, O. S. Overcoming evolved resistance to population-suppressing homing-based gene drives. Sci. Rep. 7, 3776. https://doi.org/10.1038/s41598-017-02744-7 (2017).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    38.
    Eckhoff, P. A., Wenger, E. A., Godfray, H. C. & Burt, A. Impact of mosquito gene drive on malaria elimination in a computational model with explicit spatial and temporal dynamics. Proc. Natl. Acad. Sci. U.S.A. 114, E255–E264. https://doi.org/10.1073/pnas.1611064114 (2017).
    CAS  Article  PubMed  Google Scholar 

    39.
    North, A., Burt, A. & Godfray, H. C. Modelling the spatial spread of a homing endonuclease gene in a mosquito population. J. Appl. Ecol. 50, 1216–1225. https://doi.org/10.1111/1365-2664.12133 (2013).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    40.
    Kirk, N., Kannemeyer, R., Greenaway, A., MacDonald, E. & Stronge, D. Understanding attitudes on new technologies to manage invasive species. Pac. Conserv. Biol. https://doi.org/10.1071/pc18080 (2019).
    Article  Google Scholar 

    41.
    Mercier, O. R., KingHunt, A. & Lester, P. J. Novel biotechnologies for eradicating wasps: seeking Māori studies students’ perspectives with Q method. Kōtuitui N. Z. J. Soc. Sci. 14, 136–156. https://doi.org/10.1080/1177083x.2019.1578245 (2019).
    Article  Google Scholar 

    42.
    Peters, R. S. et al. Evolutionary history of the Hymenoptera. Curr. Biol. 27, 1013–1018. https://doi.org/10.1016/j.cub.2017.01.027 (2017).
    CAS  Article  PubMed  Google Scholar 

    43.
    Stein, K. J. & Fell, R. D. Correlation of queen sperm content with colony size in yellowjackets (Hymenoptera: Vespidae). Environ. Entomol. 23, 1497–1500. https://doi.org/10.1093/ee/23.6.1497 (1994).
    Article  Google Scholar 

    44.
    Lester, P. J., Haywood, J., Archer, M. E. & Shortall, C. R. The long-term population dynamics of common wasps in their native and invaded range. J. Anim. Ecol. 86, 337–347. https://doi.org/10.1111/1365-2656.12622 (2017).
    Article  PubMed  Google Scholar 

    45.
    Burt, A. & Deredec, A. Self-limiting population genetic control with sex-linked genome editors. Proc. R. Soc. B https://doi.org/10.1098/rspb.2018.0776 (2018).
    Article  PubMed  Google Scholar 

    46.
    Prowse, T. A., Adikusuma, F., Cassey, P., Thomas, P. & Ross, J. V. A Y-chromosome shredding gene drive for controlling pest vertebrate populations. eLife 8, e41873. https://doi.org/10.7554/eLife.41873 (2019).
    Article  PubMed  PubMed Central  Google Scholar 

    47.
    Li, J. et al. Can CRISPR gene drive work in pest and beneficial haplodiploid species?. Evol. Appl. https://doi.org/10.1111/eva.13032 (2020).
    Article  PubMed  PubMed Central  Google Scholar 

    48.
    Esvelt, K. M. & Gemmell, N. J. Conservation demands safe gene drive. PLoS Biol. 15, e2003850. https://doi.org/10.1371/journal.pbio.2003850 (2017).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    49.
    Piaggio, A. J. et al. Is it time for synthetic biodiversity conservation?. Trends Ecol. Evol. 32, 97–107. https://doi.org/10.1016/j.tree.2016.10.016 (2017).
    Article  PubMed  Google Scholar 

    50.
    Edgington, M. P., Harvey-Samuel, T. & Alphey, L. Population-level multiplexing, a promising strategy to manage the evolution of resistance against gene drives targeting a neutral locus. Evol. Appl. https://doi.org/10.1111/eva.12945 (2020).
    Article  Google Scholar 

    51.
    Sumner, S., Law, G. & Cini, A. Why we love bees and hate wasps. Ecol. Entomol. 43, 836–845. https://doi.org/10.1111/een.12676 (2018).
    Article  Google Scholar 

    52.
    Southon, R. J., Fernandes, O. A., Nascimento, F. S. & Sumner, S. Social wasps are effective biocontrol agents of key lepidopteran crop pests. Proc. R. Soc. B https://doi.org/10.1098/rspb.2019.1676 (2019).
    Article  PubMed  Google Scholar 

    53.
    Harris, R. J., Thomas, C. D. & Moller, H. The influence of habitat use and foraging on the replacement of one introduced wasp species by another in New Zealand. Ecol. Entomol. 16, 441–448. https://doi.org/10.1111/j.1365-2311.1991.tb00237.x (1991).
    Article  Google Scholar 

    54.
    Lester, P. J. et al. Critical issues facing New Zealand entomology. N. Z. Entomol. 37, 1–13. https://doi.org/10.1080/00779962.2014.861789 (2014).
    Article  Google Scholar 

    55.
    Hare, K. M. et al. Intractable: species in New Zealand that continue to decline despite conservation efforts. J. R. Soc. N. Z. 49, 301–319. https://doi.org/10.1080/03036758.2019.1599967 (2019).
    Article  Google Scholar 

    56.
    Hu, X. F., Zhang, B., Liao, C. H. & Zeng, Z. J. High-Efficiency CRISPR/Cas9-mediated gene editing in honeybee (Apis mellifera) embryos. G3-Genes Genom. Genet. 9, 1759–1766. https://doi.org/10.1534/g3.119.400130 (2019).
    CAS  Article  Google Scholar 

    57.
    Yan, H. et al. An engineered orco mutation produces aberrant social behavior and defective neural development in ants. Cell 170, 736-747 e739. https://doi.org/10.1016/j.cell.2017.06.051 (2017).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    58.
    Oksanen, J. et al. vegan: community ecology package. (R package version 2.4-0. https://CRAN.R-project.org/package=vegan, 2016). More