Ecology

Kim, J. K., Choi, M. B. & Moon, T. Y. Occurrence of Vespa velutina Lepeletier from Korea, and a revised key for Korean Vespa species (Hymenoptera: Vespidae). Entomol. Res. 36, 112–115 (2006).
Google Scholar 
Choi, M. B., Martin, S. J. & Lee, J. W. Distribution, spread, and impact of the invasive hornet Vespa velutina in South Korea. J. Asia-Pac. Entomol. 15, 473–477 (2012).
Google Scholar 
Do, Y. et al. Quantitative analysis of research topics and public concern on V. velutina as invasive species in Asian and European countries. Entomol. Res. 49, 456–461 (2019).
Google Scholar 
Kwon, O. & Choi, M. B. Interspecific hierarchies from aggressiveness and body size among the invasive alien hornet, Vespa velutina nigrithorax, and five native hornets in South Korea. PLoS ONE 15, e0226934 (2020).CAS 
PubMed 
PubMed Central 

Google Scholar 
Choi, M. B. Foraging behavior of an invasive alien hornet (Vespa velutina) at Apis mellifera hives in Korea: Foraging duration and success. Entomol. Res. 51, 143–148 (2021).
Google Scholar 
Turchi, L. & Derijard, B. Options for the biological and physical control of Vespa velutina nigrithorax (Hym.: Vespidae) in Europe: A review. J. Appl. Entomol. 142, 553–562 (2018).CAS 

Google Scholar 
Bessa, A. S., Carvalho, J., Gomes, A. & Santarém, F. Climate and land-use drivers of invasion: Predicting the expansion of Vespa velutina nigrithorax into the Iberian Peninsula. Insect Conserv. Divers. 9, 27–37 (2016).
Google Scholar 
Rodríguez-Flores, M. S., Seijo-Rodríguez, A., Escuredo, O. & del Carmen Seijo-Coello, M. Spreading of Vespa velutina in northwestern Spain: Influence of elevation and meteorological factors and effect of bait trapping on target and non-target living organisms. J. Pest Sci. 92, 557–565 (2019).
Google Scholar 
Robinet, C., Darrouzet, E. & Suppo, C. Spread modelling: A suitable tool to explore the role of human-mediated dispersal in the range expansion of the yellow-legged hornet in Europe. Int. J. Pest Manag. 65, 258–267 (2019).
Google Scholar 
Saunders, D. A., Hobbs, R. J. & Margules, C. R. Biological consequences of ecosystem fragmentation: A review. Conserv. Biol. 5, 18–32 (1991).
Google Scholar 
Ellstrand, N. C. & Elam, D. R. Population genetic consequences of small population size: Implications for plant conservation. Annu. Rev. Ecol. Evol. Syst. 24, 217–242 (1993).
Google Scholar 
Young, A., Boyle, T. & Brown, T. The population genetic consequences of habitat fragmentation for plants. Trends Ecol. Evol. 11, 413–418 (1996).CAS 
PubMed 

Google Scholar 
Hughes, A. R. & Stachowicz, J. J. Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proc. Natl. Acad. Sci. 101, 8998–9002 (2004).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Dudley, R. The Biomechanics of Insect Flight: Form, Function, Evolution (Princeton University Press, 2002).
Google Scholar 
Porporato, M., Manino, A., Laurino, D. & Demichelis, D. Vespa velutina Lepeletier (Hymenoptera Vespidae): A first assessment 2 years after its arrival in Italy. Redia 97, 189–194 (2014).
Google Scholar 
Sauvard, D., Imbault, V. & Darrouzet, É. Flight capacities of yellow-legged hornet (Vespa velutina nigrithorax, Hymenoptera: Vespidae) workers from an invasive population in Europe. PLoS ONE 13, e0198597 (2018).PubMed 
PubMed Central 

Google Scholar 
Monceau, K., Bonnard, O., Moreau, J. & Thiéry, D. Spatial distribution of Vespa velutina individuals hunting at domestic honeybee hives: Heterogeneity at a local scale. Insect Sci. 21, 765–774 (2014).PubMed 

Google Scholar 
Choi, M. B., Lee, S. A., Suk, H. Y. & Lee, J. W. Microsatellite variation in colonizing populations of yellow-legged Asian hornet, Vespa velutina nigrithorax, South Korea. Entomol. Res. 43, 208–214 (2013).
Google Scholar 
Jeong, J. S. et al. Tracing the invasion characteristics of the yellow-legged hornet, Vespa velutina nigrithorax (Hymenoptera: Vespidae), in Korea using newly detected variable mitochondrial DNA sequences. J. Asia-Pac. Entomol. 24(2), 135–147 (2021).MathSciNet 

Google Scholar 
Villemant, C. et al. Predicting the invasion risk by the alien bee-hawking Yellow-legged hornet Vespa velutina nigrithorax across Europe and other continents with niche models. Biol. Conserv. 144, 2142–2150 (2011).
Google Scholar 
Kishi, S. & Goka, K. Review of the invasive yellow-legged hornet, Vespa velutina nigrithorax (Hymenoptera: Vespidae), in Japan and its possible chemical control. Appl. Entomol. Zool. 52, 361–368 (2017).
Google Scholar 
Arca, M. et al. Development of microsatellite markers for the yellow-legged Asian hornet, Vespa velutina, a major threat for European bees. Conserv. Genet. Resour. 4, 283–286 (2012).
Google Scholar 
Rousset, F. genepop’007: A complete re-implementation of the genepop software for Windows and Linux. Mol. Ecol. Res. 8, 103–106 (2008).
Google Scholar 
Peakall, P. & Smouse, R. GenAlEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research—An update. Bioinformatics 28, 2537 (2012).CAS 
PubMed 
PubMed Central 

Google Scholar 
Excoffier, L. & Lischer, H. E. 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 (2010).PubMed 
PubMed Central 

Google Scholar 
Hammer, Ø., Harper, D. A. & Ryan, P. D. PAST: Paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4, 9 (2001).
Google Scholar 
Oksanen, J. et al. The vegan package. 10, 719 (2007).Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).CAS 
PubMed 
PubMed Central 

Google Scholar 
Evanno, G., Regnaut, S. & Goudet, S. Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Mol. Ecol. Resour. 14, 2611–2620 (2005).CAS 

Google Scholar 
Earl, D. A. STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4, 359–361 (2012).
Google Scholar 
Jombart, T., Devillard, S. & Balloux, F. Discriminant analysis of principal components: A new method for the analysis of genetically structured populations. BMC Genet. 11, 94 (2010).PubMed 
PubMed Central 

Google Scholar 
Jombart, T. Adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405 (2008).CAS 
PubMed 
PubMed Central 

Google Scholar 
Waraniak, J. M., Fisher, J. D., Purcell, K., Mushet, D. M. & Stockwell, C. A. Landscape genetics reveal broad and fine-scale population structure due to landscape features and climate history in the northern leopard frog (Rana pipiens) in North Dakota. Ecol. Evol. 9, 1041–1060 (2019).PubMed 
PubMed Central 

Google Scholar 
Rohlf, F. J. tpsDig, version 2.10. http://life.bio.sunysb.edu/morph/index.html (2006).Zimmermann, G. et al. Geometric morphometrics of carapace of Macrobrachium australe (Crustacea: Palaemonidae) from Reunion Island. Acta Zool. 93, 492–500 (2012).
Google Scholar  More

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain
the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in
Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles
and JavaScript. More

Mikusiński, G., Roberge, J. M. & Fuller, R. J. Ecology and Conservation of Forest Birds (Cambridge University Press, 2018).Book 

Google Scholar 
Newton, I. The role of nest sites in limiting the numbers of hole-nesting birds: a review. Biol. Conserv. 70, 265–276. https://doi.org/10.1016/0006-3207(94)90172-4 (1994).Article 

Google Scholar 
Korpimäki, E. & Hakkarainen, H. The Boreal Owl: Ecology, Behaviour and Conservation of a Forest-Dwelling Predator (Cambridge University Press, 2012).Book 

Google Scholar 
Glutz von Blotzheim, U. N. & Bauer, K. M. Handbuch der Vögel Mitteleuropas. Band 9. (Akademische Verlagsgesellschaft, 1980).Newton, I. Population Limitation in Birds (Academic press, 1998).
Google Scholar 
Moning, C. & Müller, J. Environmental key factors and their thresholds for the avifauna of temperate montane forests. For. Ecol. Manag. 256, 1198–1208. https://doi.org/10.1016/j.foreco.2008.06.018 (2008).Article 

Google Scholar 
Walankiewicz, W., Czeszczewik, D., Stański, T., Sahel, M. & Ruczyński, I. Tree cavity resources in spruce-pine managed and protected stands of the Białowieża Forest, Poland. Nat. Areas J. 34, 423–428. https://doi.org/10.3375/043.034.0404 (2014).Article 

Google Scholar 
Lambrechts, M. M. et al. The design of artificial nestboxes for the study of secondary hole-nesting birds: a review of methodological inconsistencies and potential biases. Acta Ornithol. 45, 1–26. https://doi.org/10.3161/000164510X516047 (2010).Article 

Google Scholar 
Lambrechts, M. M. et al. Nest box design for the study of diurnal raptors and owls is still an overlooked point in ecological, evolutionary and conservation studies: a review. J. Ornithol. 153, 23–34. https://doi.org/10.1007/s10336-011-0720-3 (2012).Article 

Google Scholar 
Zárybnická, M., Kubizňák, P., Šindelář, J. & Hlaváč, V. Smart nest box: a tool and methodology for monitoring of cavity-dwelling animals. Methods Ecol. Evol. 7, 483–492. https://doi.org/10.1111/2041-210X.12509 (2016).Article 

Google Scholar 
Kubizňák, P. et al. Designing network-connected systems for ecological research and education. Ecosphere 10(6), e02761. https://doi.org/10.1002/ecs2.2761 (2019).Article 

Google Scholar 
Mänd, R., Tilgar, V., Lõhmus, A. & Leivits, A. Providing nest boxes for hole-nesting birds—Does habitat matter?. Biodivers. Conserv. 14, 1823–1840. https://doi.org/10.1007/s10531-004-1039-7 (2005).Article 

Google Scholar 
König, C. & Weick, F. Owls of the World 2nd ed. (Christopher Helm, 2008).
Google Scholar 
Morelli, F., Benedetti, Y., Møller, A. P. & Fuller, R. A. Measuring avian specialization. Ecol. Evol. 9, 8378–8386. https://doi.org/10.1002/ece3.5419 (2019).Article 
PubMed 
PubMed Central 

Google Scholar 
Ševčík, R., Riegert, J., Šťastný, K., Zárybnický, J. & Zárybnická, M. The effect of environmental variables on owl distribution in Central Europe: A case study from the Czech Republic. Ecol. Inform. 64, 101375. https://doi.org/10.1016/j.ecoinf.2021.101375 (2021).Article 

Google Scholar 
Brambilla, M. et al. Species interactions and climate change: How the disruption of species co-occurrence will impact on an avian forest guild. Glob. Change Biol. 26, 1212–1224. https://doi.org/10.1111/gcb.14953 (2020).ADS 
Article 

Google Scholar 
Hayward, G. D., Hayward, P. H. & Garton, E. O. Ecology of boreal owl in the northern Rocky-Mountains, USA. Wildl. Monogr. 124, 3–59 (1993).
Google Scholar 
Zárybnická, M., Riegert, J. & Šťastný, K. The role of Apodemus mice and Microtus voles in the diet of the Tengmalm’s owl in Central Europe. Popul. Ecol. 55, 353–361. https://doi.org/10.1007/s10144-013-0367-4 (2013).Article 

Google Scholar 
Zárybnická, M., Sedláček, O., Salo, P., Šťastný, K. & Korpimäki, E. Reproductive responses of temperate and boreal Tengmalm’s owl Aegolius funereus populations to spatial and temporal variation in prey availability. Ibis 157, 369–383. https://doi.org/10.1111/ibi.12244 (2015).Article 

Google Scholar 
Mossop, D. H. The importance of old growth refugia in the Yukon boreal forest to cavity-nesting owls in Biology and Conservation of Owls of the Northern Hemisphere (eds. Duncan, J. R., Johnson, D. H. & Nicholls, T. H.) 584–586 (Forest Service General Technical Report GTR-NC-190, 1997).Domahidi, Z., Nielsen, S., Bayne, E. & Spence, J. Boreal owl (Aegolius funereus) and northern saw-whet owl (Aegolius acadicus) breeding records in managed boreal forests. Can. Field-Nat. 134, 125–131. https://doi.org/10.22621/cfn.v134i2.2146 (2020).Whitman, J. S. Diets of nesting boreal owls, Aegolius funereus, in western interior Alaska. Can. Field-Nat. 115, 476–479 (2001).
Google Scholar 
Whitman, J. S. Post-fledging estimation of annual productivity in boreal owls based on prey detritus mass. J. Raptor Res. 42, 58–60. https://doi.org/10.3356/JRR-06-88.1 (2008).Article 

Google Scholar 
Anderson, A. G. Wildfire impacts on nest provisioning and survival of Alaskan boreal owls. Master thesis, Miami University, Ohio (2017).Hayward, G. D., Steinhorst, R. K. & Hayward, P. H. Monitoring boreal owl populations with nest boxes: sample size and cost. J. Wildl. Manage. 56, 777–785. https://doi.org/10.2307/3809473 (1992).Article 

Google Scholar 
Koopman, M. E., McDonald, D. B. & Hayward, G. D. Microsatellite analysis reveals genetic monogamy among female boreal owls. J. Raptor Res. 41, 314–318. https://doi.org/10.3356/0892-1016(2007)41[314:MARGMA]2.0.CO;2 (2007).Article 

Google Scholar 
Fang, Y., Tang, S.-H., Gu, Y. & Sun, Y.-H. Conservation of Tengmalm’s owl and Sichuan wood owl in Lianhuashan Mountain, Gansu, China. Ardea 97, 649–649. https://doi.org/10.5253/078.097.0437 (2009).Article 

Google Scholar 
Löfgren, O., Hörnfeldt, B. & Carlsson, B. Site tenacity and nomadism in Tengmalm’s owl (Aegolius funereus (L.)) in relation to cyclic food production. Oecologia 69, 321–326. https://doi.org/10.1007/BF00377051 (1986).ADS 
Article 
PubMed 

Google Scholar 
Hörnfeldt, B. & Nyholm, N. E. I. Breeding performance of Tengmalm’s owl in a heavy metal pollution gradient. J. Appl. Ecol. 33, 377–386. https://doi.org/10.2307/2404759 (1996).Article 

Google Scholar 
Hipkiss, T., Hörnfeldt, B., Eklund, U. & Berlin, S. Year-dependent sex-biased mortality in supplementary-fed Tengmalm’s owl nestlings. J. Anim. Ecol. 71, 693–699. https://doi.org/10.1046/j.1365-2656.2002.t01-1-00635.x (2002).Article 

Google Scholar 
Hipkiss, T., Gustafsson, J., Eklund, U. & Hörnfeldt, B. Is the long-term decline of boreal owls in Sweden caused by avoidance of old boxes?. J. Raptor Res. 47, 15–20. https://doi.org/10.3356/JRR-11-91.1 (2013).Article 

Google Scholar 
Korpimäki, E. Selection for nest-hole shift and tactics of breeding dispersal in Tengmalm’s owl Aegolius funereus. J. Anim. Ecol. 56, 185–196. https://doi.org/10.2307/4808 (1987).Article 

Google Scholar 
Drdáková-Zárybnická, M. Breeding biology of the Tengmalm’s owl (Aegolius funereus) in air-pollution damaged areas of the Krušné hory Mts. Sylvia 39, 35–51 (2003).
Google Scholar 
Zárybnická, M., Riegert, J., Kloubec, B. & Obuch, J. The effect of elevation and habitat cover on nest box occupancy and diet composition of boreal owls Aegolius funereus. Bird Study 64, 222–231. https://doi.org/10.1080/00063657.2017.1316236 (2017).Article 

Google Scholar 
Zárybnická, M., Kloubec, B., Obuch, J. & Riegert, J. Fledgling productivity in relation to diet composition of Tengmalm’s owl Aegolius funereus in Central Europe. Ardeola 62, 163–171. https://doi.org/10.13157/arla.62.1.2015.163 (2015).Article 

Google Scholar 
Kloubec, B. Breeding of Tengmalm’s owls (Aegolius funereus) in nest-boxes in Šumava Mts.: a summary from the years 1978–2002. Buteo 13, 75–86 (2003).
Google Scholar 
Flousek, J. Ochrana sov v Krkonošském národním parku in Sovy 1986 (eds. Sitko, J. & Trpák, P.) 33–34 (Státní ústav památkové péče a ochrany přírody, Přerov, 1988).Ravussin, P.-A. et al. Quel avenir pour la Chouette de Tengmalm Aegolius funereus dans le massif du Jura? Bilan de trente années de suivi. Nos Oiseaux 62, 5–28 (2015).
Google Scholar 
Schelper, W. Zur Brutbiologie, Ernährung und Populationsdynamik des Rauhfusskauzes Aegolius funereus im Kaufunger Wald (Südniedersachsen). Vogelkundliche Berichte aus Niedersachsen 21, 33–53 (1989).
Google Scholar 
Schwerdtfeger, O. The dispersion dynamics of Tengmalm’s owl Aegolius funereus in Central Europe in Raptor Conservation Today (eds. Meyburg, B. U. & Chancellor, R. C.) 543–550 (World Working Group on Birds of Prey and Pica Press, 1994).Hunke, W. Versuch eine Population des Raufußkauzes Aegolius funereus durch Anbringen von Nistkästen in den Jahren 1980 bis 2010 zu fördern. Charadrius 47, 93–101 (2011).
Google Scholar 
Mezzavilla, F. & Lombardo, S. Indagini sulla biologia riproduttiva della civetta capogrosso Aegolius funereus: anni 1987–2012 in Atti Secondo Convegno Italiano Rapaci Diurni e Notturni Vol. 3 (eds. Mezzavilla, F. & Scarton, F.) 261–270 (Associazione Faunisti Veneti, Quaderni Faunistici, 2013).Rajković, D. Diet composition and prey diversity of Tengmalm’s owl Aegolius funereus (Linnaeus, 1758; Aves: Strigidae) in central Serbia during breeding. Turk. J. Zool. 42, 346–351. https://doi.org/10.3906/zoo-1709-28 (2018).Article 

Google Scholar 
Zárybnická, M., Riegert, J. & Šťastný, K. Non-native spruce plantations represent a suitable habitat for Tengmalm’s owl (Aegolius funereus) in the Czech Republic, Central Europe. J. Ornithol. 156, 457–468. https://doi.org/10.1007/s10336-014-1145-6 (2015).Article 

Google Scholar 
Kopáček, J. & Veselý, J. Sulfur and nitrogen emissions in the Czech Republic and Slovakia from 1850 till 2000. Atmos. Environ. 39, 2179–2188. https://doi.org/10.1016/j.atmosenv.2005.01.002 (2005).ADS 
CAS 
Article 

Google Scholar 
Kloubec, B., Hora, J. & Šťastný, K. (eds.). Ptáci jižních Čech (Jihočeský kraj, 2015).Ševčík, R., Riegert, J., Šindelář, J. & Zárybnická, M. Vocal activity of the Central European boreal owl population in relation to varying environmental conditions. Ornis Fenn. 96, 1–12 (2019).
Google Scholar 
Savický, J. AM Services – Play Spectrogram Screens v. 4v7 (Czech Republic, 2009).Korpimäki, E. Diet of breeding Tengmalm’s owls Aegolius funereus: long-term changes and year-to-year variation under cyclic food conditions. Ornis Fenn. 65, 21–30 (1988).
Google Scholar 
Kouba, M. et al. Home range size of Tengmalm’s owl during breeding in Central Europe is determined by prey abundance. PLoS ONE 12, e0177314. https://doi.org/10.1371/journal.pone.0177314 (2017).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Zárybnická, M., Sedláček, O. & Korpimäki, E. Do Tengmalm’s owls alter parental feeding effort under varying conditions of main prey availability?. J. Ornithol. 150, 231–237. https://doi.org/10.1007/s10336-008-0342-6 (2009).Article 

Google Scholar 
R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, Austria, 2020).ter Braak, C. & Šmilauer, P. Canoco Reference Manual and User’s Guide: Software for Ordination, version 5.10. (Microcomputer Power, 2018).Kosiński, Z. & Kempa, M. Density, distribution and nest-sites of woodpeckers Picidae, in a managed forest of Western Poland. Pol. J. Ecol. 55, 519–533 (2007).
Google Scholar 
Miller, K. E. Nest-site limitation of secondary cavity-nesting birds in even-age southern pine forests. Wilson J. Ornithol. 122, 126–134. https://doi.org/10.1676/07-130.1 (2010).Article 

Google Scholar 
Sonerud, G. A. Nest hole shift in Tengmalm’s owl Aegolius funereus as defence against nest predation involving long-term memory in the predator. J. Anim. Ecol. 54, 179–192. https://doi.org/10.2307/4629 (1985).Article 

Google Scholar 
Sonerud, G. A. Reduced predation by pine martens on nests of Tengmalm’s owl in relocated boxes. Anim. Behav. 37, 332–334. https://doi.org/10.1016/0003-3472(89)90122-X (1989).Article 

Google Scholar 
Sonerud, G. A. Win – and stay, but not too long: cavity selection by boreal owls to minimize nest predation by pine marten. J. Ornithol. 162, 839–855. https://doi.org/10.1007/s10336-021-01876-y (2021).Article 

Google Scholar 
Korpimäki, E. Does nest-hole quality, poor breeding success or food depletion drive the breeding dispersal of Tengmalm’s owls?. J. Anim. Ecol. 62, 606–613. https://doi.org/10.2307/5382 (1993).Article 

Google Scholar 
Hruška, F. The boreal owl (Aegolius funereus) – breeding distribution, numbers, ringing results and notes on the breeding biology and feeding ecology of this species in the central part of the Jihlavské vrchy Hills. Crex 38, 112–150 (2020).
Google Scholar 
Broughton, R. et al. Nest-site competition between bumblebees (Bombidae), social wasps (Vespidae) and cavity-nesting birds in Britain and the Western Palearctic. Bird Study 62, 427–437. https://doi.org/10.1080/00063657.2015.1046811 (2015).Article 

Google Scholar 
Pawlikowski, T. & Pawlikowski, K. Nesting interactions of the social wasp Dolichovespula saxonica [F.] (Hymenoptera: Vespinae) in wooden nest boxes for birds in the forest reserve „Las Piwnicki” in the Chełmno Land (Northern Poland). Ecol. Quest. 13, 67–72. https://doi.org/10.2478/v10090-010-0017-9 (2010).Langowska, A., Ekner-Grzyb, A., Skórka, P., Tobółka, M. & Tryjanowski, P. Nest-site tenacity and dispersal patterns of Vespa crabro colonies located in bird nest-boxes. Sociobiology 56, 375–382 (2010).
Google Scholar 
Meyer, W. Mit welchem Erfolg nutzt der Rauhfusskauz Aegolius funereus (L.) Natruhölen und Nistkästen zur Brut. Vogelwelt 124, 325–331 (2003).
Google Scholar 
López, B. C. et al. Nest-box use by boreal owls (Aegolius funereus) in the Pyrenees Mountains in Spain. J. Raptor Res. 44, 40–49. https://doi.org/10.3356/JRR-09-32.1 (2010).ADS 
Article 

Google Scholar 
Zárybnická, M., Riegert, J. & Kouba, M. Indirect food web interactions affect predation of Tengmalm’s owls Aegolius funereus nests by pine martens Martes martes according to the alternative prey hypothesis. Ibis 157, 459–467. https://doi.org/10.1111/ibi.12265 (2015).Article 

Google Scholar 
Zárybnická, M. & Vojar, J. Effect of male provisioning on the parental behavior of female boreal owls Aegolius funereus. Zool. Stud. 52, 36. https://doi.org/10.1186/1810-522X-52-36 (2013).Article 

Google Scholar 
Llambías, P. & Fernandez, G. Effects of nestboxes on the breeding biology of southern house wrens Troglodytes aedon bonariae in the southern temperate zone. Ibis 151, 113–121. https://doi.org/10.1111/j.1474-919X.2008.00868.x (2009).Article 

Google Scholar 
Vrezec, A. Breeding density and altitudinal distribution of the Ural, tawny, and boreal owls in North Dinaric Alps (Central Slovenia). J. Raptor Res. 37, 55–62 (2003).
Google Scholar  More

Van Gossum, H., Sherratt, T. N., Cordero-Rivera, A. & Córdoba-Aguilar, A. The evolution of sex-limited colour polymorphism. In Dragonflies and Damselflies: Model Organisms for Ecological and Evolutionary Research (ed. Córdoba-Aguilar, A.) 219–231 (Oxford University Press, 2008).
Google Scholar 
Hughes, J. M. & Jones, M. P. Shell colour polymorphism in a mangrove snail Littorina sp. (Prosobranchia: Littorinidae). Biol. J. Linn. Soc. 25, 365–378 (1985).
Google Scholar 
Sinervo, B., Bleay, C. & Adamopoulou, C. Social causes of correlational selection and the resolution of a heritable throat color polymorphism in a lizard. Evolution 55, 2040–2052 (2001).CAS 
PubMed 

Google Scholar 
Westerman, E. L. et al. Does male preference play a role in maintaining female limited polymorphism in a Batesian mimetic butterfly? Behav. Process. 150, 47–58 (2018).CAS 

Google Scholar 
Vane-Wright, R. I. An integrated classification for polymorphism and sexual dimorphism in butterflies. J. Zool. 177, 329–337 (1975).
Google Scholar 
Timmermans, M. J., Srivathsan, A., Collins, S., Meier, R. & Vogler, A. P. Mimicry diversification in Papilio dardanus via a genomic inversion in the regulatory region of engrailed–invected. Proc. R. Soc. B 287, 20200443 (2020).CAS 
PubMed 
PubMed Central 

Google Scholar 
Brodie, E. D. III. & Janzen, F. J. Experimental studies of coral snake mimicry: Generalized avoidance of ringed snake patterns by free-ranging avian predators. Funct. Ecol. 9, 186–190 (1995).
Google Scholar 
Banci, K. R., Eterovic, A., Marinho, P. S. & Marques, O. A. Being a bright snake: Testing aposematism and mimicry in a neotropical forest. Biotropica 52, 1229–1241 (2020).
Google Scholar 
Wüster, W. et al. Do aposematism and Batesian mimicry require bright colours? A test, using European viper markings. Proc. R. Soc. B 271, 2495–2499 (2004).PubMed 
PubMed Central 

Google Scholar 
Valkonen, J. K. & Mappes, J. Resembling a viper: Implications of mimicry for conservation of the endangered smooth snake. Conserv. Biol. 28, 1568–1574 (2014).PubMed 

Google Scholar 
Sinervo, B. & Lively, C. M. The rock–paper–scissors game and the evolution of alternative male strategies. Nature 380, 240–243 (1996).ADS 
CAS 

Google Scholar 
Moon, R. M. & Kamath, A. Re-examining escape behaviour and habitat use as correlates of dorsal pattern variation in female brown anole lizards, Anolis sagrei (Squamata: Dactyloidae). Biol. J. Linn. Soc. 126, 783–795 (2019).
Google Scholar 
Le Rouzic, A., Hansen, T. F., Gosden, T. P. & Svensson, E. I. Evolutionary time-series analysis reveals the signature of frequency-dependent selection on a female mating polymorphism. Am. Nat. 185, E182–E196 (2015).PubMed 

Google Scholar 
Udyawer, V. et al. Future directions in the research and management of marine snakes. Front. Mar. Sci. 5, 399 (2018).
Google Scholar 
Goiran, C., Bustamante, P. & Shine, R. Industrial melanism in the seasnake Emydocephalus annulatus. Curr. Biol. 27, 2510–2513 (2017).CAS 
PubMed 

Google Scholar 
Goiran, C., Brown, G. P. & Shine, R. Niche partitioning within a population of sea snakes is constrained by ambient thermal homogeneity and small prey size. Biol. J. Linn. Soc. 129, 644–651 (2020).
Google Scholar 
Shine, R., Shine, T. & Shine, B. Intraspecific habitat partitioning by the sea snake Emydocephalus annulatus (Serpentes, Hydrophiidae): The effects of sex, body size, and colour pattern. Biol. J. Linn. Soc. 80, 1–10 (2003).
Google Scholar 
Udyawer, V., Goiran, C. & Shine, R. Peaceful coexistence between people and deadly wildlife: why are recreational users of the ocean so rarely bitten by sea snakes? People Nat. 3, 335–346 (2021).
Google Scholar 
Heatwole, H. Sea Snakes 2nd edn. (Krieger Publishing, 1999).
Google Scholar 
Shine, R., Shine, T. G., Brown, G. P. & Goiran, C. Life history traits of the sea snake Emydocephalus annulatus, based on a 17-yr study. Coral Reefs 39, 1407–1414 (2020).
Google Scholar 
Goiran, C., Dubey, S. & Shine, R. Effects of season, sex and body size on the feeding ecology of turtle-headed sea snakes (Emydocephalus annulatus) on IndoPacific inshore coral reefs. Coral Reefs 32, 527–538 (2013).ADS 

Google Scholar 
Olsson, M., Stuart-Fox, D. & Ballen, C. Genetics and evolution of colour patterns in reptiles. Semin. Cell Dev. Biol. 24, 529–541 (2013).PubMed 

Google Scholar 
Shine, R., Brischoux, F. & Pile, A. J. A seasnake’s colour affects its susceptibility to algal fouling. Proc. R. Soc. B 277, 2459–2464 (2010).CAS 
PubMed 
PubMed Central 

Google Scholar 
White, G. C. & Burnham, K. P. Program MARK: Survival estimation from populations of marked animals. Bird Study 46, S120–S139 (1999).
Google Scholar 
Packard, G. C. & Boardman, T. J. The misuse of ratios, indices, and percentages in ecophysiological research. Physiol. Zool. 61, 1–9 (1988).
Google Scholar 
Lukoschek, V. & Shine, R. Sea snakes rarely venture far from home. Ecol. Evol. 2, 1113–1121 (2012).PubMed 
PubMed Central 

Google Scholar 
Shine, R. All at sea: Aquatic life modifies mate-recognition modalities in sea snakes (Emydocephalus annulatus, Hydrophiidae). Behav. Ecol. Sociobiol. 57, 591–598 (2005).
Google Scholar 
Shine, R., Shine, T. G., Brown, G. P. & Goiran, C. Population dynamics of the sea snake Emydocephalus annulatus (Elapidae, Hydrophiinae). Sci. Rep. 11, 20701 (2021).ADS 

Google Scholar 
Rancurel, P. & Intes, A. Le requin tigre, Galeocerdo cuvieri Lacepede, des eaux neocaledoniennes examen des contenus stomacaux. Tethys 10, 195–199 (1982).
Google Scholar 
Heatwole, H. Predation on sea snakes. In The Biology of Sea Snakes (ed. Dunson, W. A.) 233–250 (University Park Press, 1975).
Google Scholar 
Ineich, I. & Laboute, P. Les serpents marins de Nouvelle-Calédonie (IRD éditions, 2002).
Google Scholar 
Kerford, M. R., Wirsing, A. J., Heithaus, M. R. & Dill, L. M. Danger on the rise: diurnal tidal state mediates an exchange of food for safety by the bar-bellied sea snake Hydrophis elegans. Mar. Ecol. Progr. Ser. 358, 289–294 (2008).ADS 

Google Scholar 
Masunaga, G., Kosuge, T., Asai, N. & Ota, H. Shark predation of sea snakes (Reptilia: Elapidae) in the shallow waters around the Yaeyama Islands of the southern Ryukyus, Japan. Mar. Biodivers. Rec. 1, e96 (2008).
Google Scholar 
Wirsing, A. J. & Heithaus, M. R. Olive-headed sea snakes Disteria major shift seagrass microhabitats to avoid shark predation. Mar. Ecol. Progr. Ser. 387, 287–293 (2009).ADS 

Google Scholar 
Goiran, C. & Shine, R. The ability of damselfish to distinguish between dangerous and harmless sea snakes. Sci. Rep. 10, 1377 (2020).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Norman, M. D., Finn, J. & Tregenza, T. Dynamic mimicry in an Indo-Malayan octopus. Proc. R. Soc. B 268, 1755–1758 (2001).CAS 
PubMed 
PubMed Central 

Google Scholar 
Pernetta, J. C. Observations on the habits and morphology of the sea snake Laticauda colubrina (Schneider) in Fiji. Can. J. Zool. 55, 1612–1619 (1977).
Google Scholar 
Randall, J. E. A review of mimicry in marine fishes. Zool. Stud. 44, 299–328 (2005).
Google Scholar 
Dudgeon, C. L. & White, W. T. First record of potential Batesian mimicry in an elasmobranch: Juvenile zebra sharks mimic banded sea snakes? Mar. Freshw. Res. 63, 545–551 (2012).
Google Scholar 
Sullivan Caldwell, G. & Wolff Rubinoff, R. Avoidance of venomous sea snakes by naive herons and egrets. Auk 100, 195–198 (1983).
Google Scholar 
Sanders, K. L., Malhotra, A. & Thorpe, R. S. Evidence for a Müllerian mimetic radiation in Asian pitvipers. Proc. R. Soc. B 273, 1135–1141 (2006).CAS 
PubMed 
PubMed Central 

Google Scholar 
Raveendran, D. K., Deepak, V., Smith, E. N. & Smart, U. A new colour morph of Calliophis bibroni (Squamata: Elapidae) and evidence for Müllerian mimicry in Tropical Indian coral snakes. Herpetol. Notes 10, 209–217 (2017).
Google Scholar  More

Chemicals and materialsAnalytical standard ( > 99% purity) of spiromesifen, BSN2060-enol, and chromafenozide were purchased from AB Solution Co., Ltd., Hwaseong-si, Gyeonggi-do, Republic of Korea. HPLC grade water and acetonitrile were supplied by Merck, Darmstadt, Germany. QuEChERS kit (4.0 g magnesium sulfate, 1.0 g sodium chloride, 1.0 g sodium citrate tribasic dihydrate, 0.5 g disodium citrate sesquihydrate) were obtained from Phenomenex, California, USA. Individual stock solutions of the target compounds were prepared in acetonitrile and stored at − 20 °C before use.Field experimentsThe trials were carried out in a greenhouse farm during the season 2018 at two different sites (with approximately 24 km distance between both sites) located in Chuncheon and Hongcheon-gun, Gangwon-do, Republic of Korea following the method described by the Organization for Economic Co-operation and Development (OECD)38. The field test of lettuce (Latuca sativa L.) crop was conducted in Chuncheon city, and perilla (Perilla frutescens (L.) Britton) crop in Hongcheon city. The area of each field was divided into two plots (treatment and control). The treatment plots were further divided into three replicates (subplots 33 m2). The control plot was separated by a buffer zone of 3 m2 from the treated site. To minimize spray overlap, buffer zones (1 m) were set up between subplots. The commercial products of spiromesifen 20% SC diluted 2000 times and chromafenozide 5% EC diluted 1000 times were sprayed twice at 7-days intervals using an automatic sprayer. After the second spray samples (lettuce and perilla leaves) were collected from each subplot at 0 (2 h after spraying), 1, 3, 5, and 7 days according to the Korean RDA23 method. Thirty samples 1.0 kg each from the collected crop were placed in polyethylene bag and labeled. After collection, the samples were transported to the laboratory, where they were chopped and homogenized. The homogenized samples were kept frozen at − 20 °C until analysis.We confirm all plant samples used in the current work comply with the IUCN Policy Statement on Research Involving Species at Risk of Extinction and the Convention on the Trade in Endangered Species of Wild Fauna and Flora.Samples pretreatmentA QuEChERS method was used for the extraction of the targeted compounds from lettuce and perilla leaves. A 10 g of previously homogenized samples were weighed into a 50 mL polypropylene centrifuge tube and mixed with 10 mL of water followed by 10 mL of acetonitrile. The samples were shaken at 1500 rpm in a shaker machine for 10 min. Then commercial QuEChERS kit was added, and the mixtures were shaken vigorously for 2 min in a shaker. Subsequently, the samples were centrifuged at 3584 g-force for 10 min. After centrifugation, the supernatant was filtered with a 0.22 μm membrane filter and transferred into the glass vial for instrumental analysis.LC-MS/MS analysisQuantitative determination of the tested compounds was carried out by using HPLC system Dionex Ultimate 3000 (Thermo Science, USA) coupled with tandem mass spectrometry (MS/MS) (TSQ Quantum Access Max (Thermo Science, USA). Water (solvent A) and acetonitrile (solvent B) containing 0.1% formic acid and 5 mM ammonium format were used as mobile phase at a flow rate of 0.4 mL/min and injection volume 1.0 µL. To obtain desirable chromatographic peaks, two different instrumental conditions were used. The chromatographic separation of spiromesifen was separated by Capcell core-C18 (2.1 mm I.D. × 150 mm × 2.7 μm, Shiseido Co., Ltd., Tokyo, Japan) and BSN2060-enol was performed by C18 column (Poroshell 120 SB-Ag, 2.1 mm I.D. × 100 mm × 2.7-μm, Agilent Technologies, Santa Clara, California, USA) with a gradient elution as follows (mobile phase B%): 0.0 min, 5.0%; 2.0 min 5%; 2.5 min, 95%; 6.0 min, 95%; 6.5 min, 5.0%; 10 min, 5.0%. Likewise, chromafenozide was separated by C18 column (Imtakt Unison UK-C18, 2.0 mm I.D. × 100 mm × 3.0-μm, Imtakt, Portland, USA) with a gradient elution as follows (mobile phase B%): 0.0 min, 5%; 1.0 min, 5.0%; 1.5 min, 90%; 5.0 min, 90%; 7.0 min, 5.0%; 10 min, 5.0%. An MS/MS system (TSQ quantum ultra, Thermo Science, USA) equipped with an electrospray ionization source operating in positive mode (ESI+) was used. The MS/MS parameters and selected product ions are shown in supplementary Tables S2 and S3.The calculation of spiromesifen total residuesThe total residues in lettuce and perilla samples were calculated using Eq. (1)23.Total residues of spiromesifen (mg/kg) = spiromesifen + (BSN2060 residue × 1.36). The conversion factor was calculated as follow;$${1}.{36},{text{(conversion}},{text{factor)}} = frac{{370.49left( {{text{spiromesifen}},{text{MW}}} right)}}{{272.34{ }left( {{text{BSN}}2060,{text{MW}}} right)}}$$
(1)
where MW molecular weight.Initial deposition calculationThe initial residues of spiromesifen and chromafenozide deposition in lettuce and perilla leaves were calculated from 0-day according to Eq. (2) described by Kang et al.12 as follow;$${text{A }},({text{mg}}/{text{kg}}) = {text{B(mg}}/{text{kg)}} times frac{100}{{{text{C}}({text{% }})}} times frac{1}{{text{E}}} times 1000$$
(2)
A: Initial residue (mg/kg), B: Residues (mg/kg) on 0 day, C: active ingredients, E: dilution factor.Method validationThe analytical method was validated in terms of different performance criteria such as linearity, accuracy, precision, and method limit of quantitation (MLOQ). Matrix-matched standards were used to construct the calibration curve by evaporating (0.01, 0.05, 0.1, 0.2, 0.5, 0.7 and 1.0 mg/kg) working solution (1 mL) and re-dissolved in the extract of control sample. The linearity of the matrix-matched calibration curve was evaluated by the values of the correlation coefficient (R2). The accuracy and precision were obtained in terms of recovery (70–120%) and repeatability (n = 3). The recoveries were determined by spiking the analytes at two concentrations levels (0.1 mg/L) and (0.5 mg/L) in 10 g control samples and were quantified by comparing the response of analytes in samples with response in calibration standard solutions prepared in matrix. The repeatability expressed as the relative standard deviation (RSD) of the analyzed samples was calculated from three repetitions. The MLOQ was calculated by Eq. (3) taking into consideration the following factors: the instrument limit of detection, volume of extraction solvent, injection volume, dilution factor, and sample amount39,40.$${text{MLOQ}},{text{(mg}}/{text{kg)}} = {text{A(ng)}} times frac{{text{B(mL)}}}{{{text{C(}}upmu {text{L)}}}} times frac{{text{D}}}{{text{E(g)}}}$$
(3)
where A: instrument limit of detection, B: volume of extraction solvent, C: injection volume, D: dilution factor, E: sample amount.Half-life calculationThe dissipation patterns of spiromesifen and chromafenozide in lettuce and perilla leaves over time were found following the first-order kinetics model28. The half-life was determined by the following equation:$${text{C}}_{{text{t}}} = {text{C}}_{0} times {text{e}}^{{ – {text{kt}}}} ,{text{DT}}_{{{5}0}} = {text{ln2}}/{text{k}}$$where Ct is the concentration of the insecticide, C0 represents the initial residue concentration of insecticide, t is the time (days) after insecticide application, and k is the constant rate.Safety assessmentIn this study, the safety assessments (percent acceptable daily intake; %ADI) of the target insecticides that are consumed with lettuce and perilla leaves were calculated by the ratio of estimated daily intake (EDI) to acceptable daily intake (ADI). The EDI was calculated using insecticide concentration and average consumption of food commodities per person per day. In addition, the theoretical maximum daily intakes (TMDIs) of both insecticides were calculated using the maximum residue limits (MRLs) and average body weight (60 kg) of adults in Republic of Korea. TMDIs were calculated following the equation described by Kim et al.41.$$begin{aligned} & {text{ADI (mg}}/{text{person}}/{text{day)}} = {text{ADI}},({text{mg}}/{text{kg}}/{text{body weight}}/{text{day}}),{text{of target insecticide}} times {text{6}}0,({text{average body weight}}) \ & {text{EDI (mg}}/{text{kg}}/{text{person)}} = {text{concentration of target insecticide (mg}}/{text{kg)}} times {text{ daily food intake (g)}} \ & % {text{ADI}} = {text{EDI}}/{text{ADI}} times {text{1}}00 \ & {text{TMDI}}% = sum % {text{ADI of all registered crops}} \ end{aligned}$$ More

German, C. R. & Von Damm, K. L. Treatise on Geochemistry (eds Heinrich, D. H. & Karl, K. T.) 181–222 (Pergamon, 2003).Van Dover, C. The Ecology of Deep-Sea Hydrothermal Vents (Princeton University Press, 2000).Spiess, F. N. et al. East Pacific rise: Hot springs and geophysical experiments. Science 207, 1421–1433 (1980).CAS 

Google Scholar 
Haymon, R. M. et al. Hydrothermal vent distribution along the East Pacific Rise crest 9° 09’–54’ N and its relationship to magmatic and tectonic processes on fast-spreading mid-ocean ridges. Earth Planetary Sci. Lett. 104, 513–534 (1991).
Google Scholar 
Edmonds, H. N. et al. Discovery of abundant hydrothermal venting on the ultraslow-spreading Gakkel Ridge in the Arctic Ocean. Nature 421, 252–256 (2003).CAS 

Google Scholar 
German, C. R. et al. Hydrothermal activity and seismicity at Teahitia Seamount: Reactivation of the society islands hotspot? Front. Mar. Sci 7, 73 (2020).
Google Scholar 
de Ronde, C. E. J. et al. Intra-oceanic subduction-related hydrothermal venting, Kermadec volcanic arc, New Zealand. Earth Planetary Sci. Lett. 193, 359–369 (2001).
Google Scholar 
Ishibashi, J. & Urabe, T. Backarc Basins: Tectonics and Magmatism (ed Taylor, B.) 451–495 (Springer, 1995).Fouquet, Y. et al. Hydrothermal activity and metallogenesis in the Lau back-arc basin. Nature 349, 778–781 (1991).CAS 

Google Scholar 
Boschen, R. E., Rowden, A. A., Clark, M. R. & Gardner, J. P. A. Mining of deep-sea seafloor massive sulfides: A review of the deposits, their benthic communities, impacts from mining, regulatory frameworks, and management strategies. Ocean Coastal Manage. 84, 54–67 (2013).
Google Scholar 
Lisitsyn, A. P. et al. Active hydrothermal activity at Franklin Seamount, Western Woodlark Sea (Papua New Guinea). Int. Geol. Rev. 33, 914–929 (1991).
Google Scholar 
Laurila, T. E. et al. Tectonic and magmatic controls on hydrothermal activity in the Woodlark Basin: Hydrothermalism in the Woodlark Basin. Geochem. Geophys. Geosyst. 13, Q09006 (2012).Goodliffe, A. M. et al. Synchronous reorientation of the Woodlark Basin spreading center. Earth Planetary Sci. Lett. 146, 233–242 (1997).CAS 

Google Scholar 
Martínez, F., Taylor, B. & Goodliffe, A. M. Contrasting styles of seafloor spreading in the Woodlark Basin: Indications of rift-induced secondary mantle convection. J. Geophys. Res. 104, 12909–12926 (1999).
Google Scholar 
Taylor, B., Goodliffe, A., Martinez, F. & Hey, R. Continental rifting and initial sea-floor spreading in the Woodlark Basin. Nature 374, 534–537 (1995).CAS 

Google Scholar 
Schellart, W. P., Lister, G. S. & Toy, V. G. A Late Cretaceous and Cenozoic reconstruction of the Southwest Pacific region: Tectonics controlled by subduction and slab rollback processes. Earth-Sci. Rev. 76, 191–233 (2006).
Google Scholar 
Hall, R. Cenozoic geological and plate tectonic evolution of SE Asia and the SW Pacific: Computer-based reconstructions, model and animations. J. Asian Earth Sci. 20, 353–431 (2002).
Google Scholar 
Breusing, C. et al. Allopatric and sympatric drivers of speciation in Alviniconcha hydrothermal vent snails. Mol. Biol. Evol. 37, 3469–3484 (2020).CAS 

Google Scholar 
Ondréas, H., Scalabrin, C., Fouquet, Y. & Godfroy, A. Recent high-resolution mapping of Guaymas hydrothermal fields (Southern Trough). BSGF – Earth Sci. Bull. 189, 6 (2018).
Google Scholar 
Nakamura, K. et al. Water column imaging with multibeam echo-sounding in the mid-Okinawa Trough: Implications for distribution of deep-sea hydrothermal vent sites and the cause of acoustic water column anomaly. Geochem. J. 49, 579–596 (2015).CAS 

Google Scholar 
Xu, G., Jackson, D. R. & Bemis, K. G. The relative effect of particles and turbulence on acoustic scattering from deep sea hydrothermal vent plumes revisited. J. Acoust. Soc. Am. 141, 1446–1458 (2017).
Google Scholar 
Park, S.-H. et al. Petrogenesis of basalts along the eastern Woodlark spreading center, equatorial western Pacific. Lithos 316–317, 122–136 (2018).
Google Scholar 
Chadwick, J. et al. Arc lavas on both sides of a trench: Slab window effects at the Solomon Islands triple junction, SW Pacific. Earth Planetary Sci. Lett. 279, 293–302 (2009).CAS 

Google Scholar 
Fouquet, Y. et al. Geodiversity of Hydrothermal Processes Along the Mid-Atlantic Ridge and Ultramafic-Hosted Mineralization: A New Type of Oceanic Cu-Zn-Co-Au Volcanogenic Massive Sulfide Deposit (eds Rona, P. A., Devey, C. W., Dyment, J. & Murton, B. J.) Vol. 188, 321–367 (American Geophysical Union, 2010).Von Damm, K. et al. Chemistry of submarine hydrothermal solutions at 21N, East Pacific Rise. Geochim. Cosmochim. Acta 49, 2197–2220 (1985).
Google Scholar 
Seyfried, W. E. & Bischoff, J. L. Experimental seawater-basalt interaction at 300 °C, 500 bars, chemical exchange, secondary mineral formation and implications for the transport of heavy metals. Geochim. Cosmochim. Acta 45, 135–147 (1981).CAS 

Google Scholar 
Pester, N. J., Rough, M., Ding, K. & Seyfried, W. E. A new Fe/Mn geothermometer for hydrothermal systems: Implications for high-salinity fluids at 13°N on the East Pacific Rise. Geochim. Cosmochim. Acta https://doi.org/10.1016/j.gca.2011.08.043 (2011).Podowski, E. L., Moore, T. S., Zelnio, K. A., Luther, G. W. & Fisher, C. R. Distribution of diffuse flow megafauna in two sites on the Eastern Lau Spreading Center, Tonga. Deep Sea Res. Part I: Oceanogr. Res. Papers 56, 2041–2056 (2009).CAS 

Google Scholar 
Collins, P., Kennedy, R. & Van Dover, C. A biological survey method applied to seafloor massive sulphides (SMS) with contagiously distributed hydrothermal-vent fauna. Mar. Ecol. Prog. Ser. 452, 89–107 (2012).CAS 

Google Scholar 
Desbruyères, D., Hashimoto, J. & Fabri, M.-C. Composition and biogeography of hydrothermal vent communities in Western Pacific back-arc basins. Geophys. Monogr. Ser. 166, 215–234 (2006).Reid, W. D. K. et al. Spatial differences in East scotia ridge hydrothermal vent food webs: Influences of chemistry, microbiology, and predation on trophodynamics. PLoS One 8, e65553 (2013).CAS 

Google Scholar 
Van Audenhaege, L., Fariñas-Bermejo, A., Schultz, T. & Lee Van Dover, C. An environmental baseline for food webs at deep-sea hydrothermal vents in Manus Basin (Papua New Guinea). Deep Sea Res. Part I: Oceanogr. Res. Papers https://doi.org/10.1016/j.dsr.2019.04.018 (2019).Erickson, K. L., Macko, S. A. & Van Dover, C. L. Evidence for a chemoautotrophically based food web at inactive hydrothermal vents (Manus Basin). Deep-Sea Res. Part II: Top. Stud. Oceanogr. 56, 1577–1585 (2009).CAS 

Google Scholar 
Comeault, A., Stevens, C. J. & Juniper, S. K. Mixed photosynthetic-chemosynthetic diets in vent obligate macroinvertebrates at shallow hydrothermal vents on Volcano 1, South Tonga Arc—evidence from stable isotope and fatty acid analyses. Cahiers de Biologie Marine 51, 351–359 (2010).
Google Scholar 
Bennett, S. A., Dover, C. V., Breier, J. A. & Coleman, M. Effect of depth and vent fluid composition on the carbon sources at two neighboring deep-sea hydrothermal vent fields (Mid-Cayman Rise). Deep-Sea Res. Part I: Oceanogr. Res. Papers 104, 122–133 (2015).CAS 

Google Scholar 
Levin, L. A. et al. Hydrothermal vents and methane seeps: Rethinking the sphere of influence. Front. Marine Sci. 3, 1–23 (2016).
Google Scholar 
Hügler, M. & Sievert, S. M. Beyond the Calvin cycle: Autotrophic carbon fixation in the ocean. Annu. Rev. Mar. Sci. 3, 261–289 (2011).
Google Scholar 
Wang, X., Li, C., Wang, M. & Zheng, P. Stable isotope signatures and nutritional sources of some dominant species from the PACManus hydrothermal area and the Desmos caldera. PLoS One 13, e0208887 (2018).
Google Scholar 
Tunnicliffe, V. & Southward, A. J. Growth and breeding of a primitive stalked barnacle Leucolepas longa (Cirripedia: Scalpellomorpha: Eolepadidae: Neolepadinae) inhabiting a volcanic seamount off Papua New Guinea. J. Mar. Biol. Ass. 84, 121–132 (2004).
Google Scholar 
Auzende, J. M., Pelletier, B. & Lafoy, Y. Twin active spreading ridges in the North Fiji Basin (southwest Pacific). Geology 22, 63–66 (1994).
Google Scholar 
Parson, L. M. & Wright, I. C. The Lau-Havre-Taupo back-arc basin: A southward-propagating, multi-stage evolution from rifting to spreading. Tectonophysics 263, 1–22 (1996).
Google Scholar 
Thaler, A. D. et al. Comparative population structure of two deep-sea hydrothermal-vent-associated decapods (Chorocaris sp. 2 and Munidopsis lauensis) from Southwestern Pacific back-arc basins. PLoS One 9, e101345 (2014).
Google Scholar 
Lee, W.-K., Kim, S.-J., Hou, B. K., Van Dover, C. L. & Ju, S.-J. Population genetic differentiation of the hydrothermal vent crab Austinograea alayseae (Crustacea: Bythograeidae) in the Southwest Pacific Ocean. PLoS One 14, e0215829 (2019).CAS 

Google Scholar 
Plouviez, S. et al. Amplicon sequencing of 42 nuclear loci supports directional gene flow between South Pacific populations of a hydrothermal vent limpet. Ecol. Evol. https://doi.org/10.1002/ece3.5235 (2019).Tran Lu Y, A. et al. Fine-scale genomic patterns of connectivity in the deep sea hydrothermal gastropod Ifremeria nautilei over its species range using outlier scans and demo-genetic inferences. Mol. Ecol. (In Revision).Yearsley, J. M. & Sigwart, J. D. Larval transport modeling of deep-sea invertebrates can aid the search for undiscovered populations. PLoS One 6, e23063 (2011).CAS 

Google Scholar 
Mitarai, S., Watanabe, H., Nakajima, Y., Shchepetkin, A. F. & McWilliams, J. C. Quantifying dispersal from hydrothermal vent fields in the western Pacific Ocean. Proc. Natl Acad. Sci. USA 113, 2976–2981 (2016).CAS 

Google Scholar 
Marsh, L. et al. Microdistribution of faunal assemblages at deep-sea hydrothermal vents in the southern ocean. PLoS One 7, e48348 (2012).CAS 

Google Scholar 
Jollivet, D. et al. The Biospeedo cruise: A new survey of hydrothermal vents along the south East Pacific Rise from 7°24’ S to 21°33’ S. InterRidge News 13, 20–26 (2005).Girard, F. et al. Currents and topography drive assemblage distribution on an active hydrothermal edifice. Prog. Oceanogr. 187, 102397 (2020).
Google Scholar 
Hessler, R. R. & Lonsdale, P. F. Biogeography of Mariana Trough hydrothermal vent communities. Deep Sea Res. Part A. Oceanogr. Res. Papers 38, 185–199 (1991).
Google Scholar 
Fujikura, K. Biology and earth scientific investigation by the submersible ‘Shinkai 6500’ system of deep-sea hydrothermal and lithosphere in the Mariana back-arc basin. JAMSTEC J. Deep Sea Res. 13, 1–20 (1997).
Google Scholar 
Connelly, D. P. et al. Hydrothermal vent fields and chemosynthetic biota on the world’s deepest seafloor spreading centre. Nat. Commun. 3, 620 (2012).
Google Scholar 
Cline, J. D. Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol. Oceanogr. 14, 454–458 (1969).CAS 

Google Scholar 
Craddock, P. R., Rouxel, O. J., Ball, L. A. & Bach, W. Sulfur isotope measurement of sulfate and sulfide by high-resolution MC-ICP-MS. Chem. Geol. 253, 102–113 (2008).CAS 

Google Scholar 
Mateo, M. A., Serrano, O., Serrano, L. & Michener, R. H. Effects of sample preparation on stable isotope ratios of carbon and nitrogen in marine invertebrates: Implications for food web studies using stable isotopes. Oecologia 157, 105–115 (2008).
Google Scholar 
Hedges, J. I. & Stern, J. H. Carbon and nitrogen determinations of carbonate-containing solids1. Limnol. Oceanogr. 29, 657–663 (1984).CAS 

Google Scholar 
Coplen, T. B. Guidelines and recommended terms for expression of stable-isotope-ratio and gas-ratio measurement results: Guidelines and recommended terms for expressing stable isotope results. Rapid Commun. Mass Spectrom. 25, 2538–2560 (2011).CAS 

Google Scholar 
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 3, 294–299 (1994).CAS 

Google Scholar 
Methou, P., Michel, L. N., Segonzac, M., Cambon-Bonavita, M.-A. & Pradillon, F. Integrative taxonomy revisits the ontogeny and trophic niches of Rimicaris vent shrimps. R. Soc. Open Sci. 7, 200837 (2020).CAS 

Google Scholar 
Leigh, J. W. & Bryant, D. Popart: Full‐feature software for haplotype network construction. Methods Ecol. Evol. 6, 1110–1116 (2015).
Google Scholar  More

Study sites and samplingWe sampled gas and soil in 29 regions throughout the A (rainy tropical), C (temperate), and D (boreal) climate types of the Köppen classification from six continents during the vegetation period between August 2011 and June 2018, following a standard protocol26. According to the protocol, the gas and soil samples were collected from locations in public domain or in previous agreement with the local community and/or property owner. The samples were exported from the origin countries and imported to Estonia, EU in cooperation with customs officers of the respective states, following the legal provisions of soil export and import, specifically exemptions for scientific purposes. To capture the full range of environmental conditions in each region, we established 76 wetland soil sites under different vegetation (mosses, sedges, grasses, herbs, trees, and bare soil) and land-use types (natural—raised bog, fen, and forest; agricultural—arable, hay field and pasture; and a peat extraction area) (Fig. 1a; Supplementary Data 1). We used a four-grade land-use intensity index to quantify the effect of land conversion: 0, no agricultural land use (natural mire, swamp, or bog forest); 1, moderate grazing or mowing (once a year or less); 2, intensive grazing or mowing (more than once a year); and 3, arable land (directly fertilized or unfertilized). The vegetation and land-use intensity types and the land-use intensity index were estimated from observations and contacts with site managers and local researchers.Within the sites, we established 1–4 stations 15–500 m apart to maximize the captured environmental variation. Each of the 196 stations were equipped with 3–5 opaque PVC 65 L truncated conical chambers 1.5–5 m apart and an observation well (perforated, 50 mm diameter PP-HT pipe wrapped in geotextile; 1 m in length). From each of the 645 chambers, N2O fluxes were measured following the static chamber method37 using PVC collars (0.5 m diameter, installed to 0.1 m depth in soil). Stabilization of 3–12 h was allowed before gas sampling to reduce the disturbance effect of inserting the collars on fluxes. The chambers were placed into water-filled rings on top of the collars. Gases were sampled from the chamber headspace into a 50 mL glass vial every 20 min during a 1-h session. The vials had been evacuated in the laboratory 2–6 days before the sampling. At least three sampling sessions per location were run within 3 days. Water-table height was recorded from the observation wells during the gas sampling at least 8 h after placement. Soil temperature was measured at the 10 and 20 cm depth.Soil samples of 150–200 g were collected from the chambers at 0–10 cm depth after the final gas sampling, and transported to laboratories in Tartu, Estonia. The homogenized samples were divided into subsamples for physical–chemical analyses and DNA extraction. The samples for chemical analyses were stored at 4 °C and microbiological samples were stored at –20 °C. DNA extraction was provided at the Tartu University environmental microbiology laboratory (see details below). Using a PP-HT plastic cylinder, intact soil cores (diameter 6.8 cm, height 6 cm) for the N2 analysis with the He–O2 method38 were collected from the topsoil (0−10 cm) inside 252 chambers at 26 sites, starting from 2014. Samples from different climates were run at respective temperatures. During transport, the soil samples were kept below the ambient soil temperature from which they were collected.Gas flux analysesThe gas samples were analyzed for N2O concentration within 2 weeks using two Shimadzu GC-2014 gas chromatographs equipped with ECD, TCD, and a Loftfield-type autosampler. The N2O fluxes were determined on linear regressions obtained from consecutive N2O concentrations taken when the chamber was closed, using p  0.05 we removed one outlier. If the regression remained insignificant but the flux value fell below the gas-chromatography measuring accuracy (regression change of N2O concentration δv  More

In the work reported here, we have examined the interaction of symbiotic partners representative of the three major diversification centers. Although P. vulgaris could establish symbiosis with diverse rhizobial lineages, Rhizobium etli seemed to predominate in nature in the bean nodules collected from the Americas8,9, while the Americas is where the origin and diversification of the host have been experimentally supported19,20. Genotypes other than R. etli that also induce nodule formation in the bean have already been taxonomically defined as species, for instance Rhizobium tropici and Rhizobium ecuadorense, both of which were isolated from areas in northwestern South America, namely Ecuador, Brazil, and Colombia.American-bean rhizobia, from soil samples retrieved by the common bean as well as isolates from nodules found in nature have possessed polymorphism in the nodC gene, disclosing three nodC genotypes namely α, (upgamma), and (updelta)9. The different nodC alleles in American strains exhibit a varying predominance in their regional distributions in correlation with the centers of bean genetic diversification. The nodC types α and (upgamma) were detected both in bean nodules and in soils from Mexico, whereas the nodC type (updelta) was clearly predominant in soil and nodules from the Southern Andes (i. e., in Bolivia and northwest Argentina9). A quantitatively balanced representation of rhizobia with nodC type α and (upgamma) was detected in soils from Ecuador, but the nodC type (upgamma) had been found to be predominantly isolated from nodules formed in nature in that area5,9,10. It should be noted that we have reported finding of equal distribution of allele nodC type α and γ among the nine R etli isolates from bean in Mexico reported by Silva et al.7,9. The occurrence of this polymorphism proved to contribute to examining rhizobial populations inhabiting the Americas and characterizing the interaction with beans in BGD centers from Mexico to the northwest of Argentina. In performing our nodC analysis, we were aware that rhizobia genes for symbiosis are carried on plasmids which might mediate horizontal transfer, however in agreement with Silva et al.7 we assumed that although genetic exchange could be important, it is not so extensive to prevent epidemic clones from arising at significant frequency. Similar findings were found in R. leguminosarum bv trifolii associated with native Trifolium species growing in nature21.Investigations in the last decade have proposed an evolutionary pathway for the host bean that provided us with a framework for examining our results on rhizobia-bean interactions and facilitated an interpretation of the results. The current model proposes the occurrence of a Mesoamerican origin from where dispersion by independent migrations over time led to the Mesoamerican and Andean gene pools and to the Ecuador-Peru wild common-bean populations2,19,20. We found a balanced competition between α and (upgamma) nodC types in beans from Mesoamerica and the southern Andes, whereas the beans from Ecuador and Peru revealed a clear affinity for nodulation with strains of nodC type α rather than with the sympatric strains nodC type (upgamma) that we assayed (R. ecuadorense, CIAT894 and Bra-5). Nevertheless, we have previously reported that native strains and isolates with respectively both nodC types α and (upgamma) were found in soils and bean nodules from Mexico9, whereas lineages harboring nodC type (upgamma) were found to be predominant in beans from the northern and central regions of Ecuador-Peru8,9. The present results, however, indicated a clear affinity of the Ecuadorean-Peruvian—i. e., AHD—beans for strains nodC type α when assessed for competition against nodC type (upgamma) (Fig. 2A). We also found that nodC type (updelta) displayed a clear predominant occupancy of nodules of the AHD beans in contrast to the scarce occupancy of nodules of the Mesoamerican and Andean beans (Fig. 2B). Taken together, these results indicate no affinity of AHD beans for sympatric rhizobial strains containing nodC type (upgamma)—despite the finding that rhizobia of nodC type (upgamma) appear to predominate in isolates of nodules formed in Ecuador9,10.We conclude that although rhizobial type nodC (upgamma) was previously found to predominate in bean nodules from Ecuador, the competitiveness of that rhizobial strain for nodulation compared to other genotypes of bean rhizobia was relatively low. A possible explanation could be that seeds might be assumed to play a key role as carriers during the dissemination of the bean throughout the American regions. Thus, we can hypothesize that at the time of bean dissemination both R. etli nodC types α and (upgamma) (R. ecuadorense and other lineages) moved in conjunction with the host from Mesoamerica to northern Ecuador-Peru, but the strains bearing nodC type (upgamma) achieved an adaptation—probably due to edaphic characteristics, environmental stresses, and other features—in such a way that that strain predominated in soils and succeeded in nodulation.Alternatively, that prevalence might arise from a host selection for a rhizobium that is more effective in nitrogen fixation in a new and different environment. A poor relationship, however, between competitiveness and efficiency was found in the pea22. In line with the concept of adaptation, the bean had been found to be preferentially nodulated by species of R. tropici in acidic soils in regions of Brazil and Africa4,23. Since the environment could also be a major influence on the host and its symbiotic interactions, the Andean area represents a cooler climate for the growth of the bean than the Mesoamerican region24,25. Furthermore, since our assays were performed in laboratory environment parameters, we do not rule out the effect -if any- by the diverse and complex soil microbial community coexisting with bean rhizobia. Within this context, two contrasting soils from Argentina which differ in geolocation and edaphic properties and the perlite substrate were assayed side by side in nodule occupancy of Negro Xamapa after inoculation with a mixture of strains nodC type α and γ (Results not shown). Our results showed that the predominance of nodC type γ in the occupation of the nodules of this variety (about 80% occupation) is not affected by the type of substrate (p = 0.5566). Yet, we assume that the performance in diverse soil and ecosystems should be further evaluated in situ. In agreement, a good coevolution of rhizobia strains with nodC type (upgamma) was detected in nodules of bean varieties from the Mesoamerica and Andean genetic pools inoculated with soil samples from Mexico, Ecuador, and Northwest of Argentina, respectively (see Table 2 in Aguilar et al., 2004) [9].With respect to the interaction in the southern Andes, we propose another interpretation that takes into consideration the bottleneck that occurred before domestication in the Andes, as was indicated by Bitocchi et al.26, which scenario enables the assumption that the adaptation and concomitant diversification involved a coevolution of the symbioses. Therefore, similar profiles of competitiveness for nodulation in Mesoamerican and Andean beans were found between nodC type (upgamma) versus nodC types α and (updelta), but a significant occupancy by the nodC type (updelta) was recorded in the Andean beans.Our work suggests that the genetics of both the host and the bacteria determine the mutual affinity and additionally indicates that symbiotic interaction is another trait of legumes sensitive to the effects of evolution and ecological adaptation to the locale environment such as the characteristics of the soil and the climate.The analysis of the genetic sequences of the bean that encode genes associated with symbiosis, revealed variation of NFR1, NFR5 and NIN over the representative accessions of the Mesoamerican, the Andean, and the AHD gene pools. It is proposed that a receptor complex composed of NFR1 and NFR5 initiates signal transduction in response to Nod-factor synthesized and released by rhizobia27. Although the variation consisted mainly in neutral-amino-acid substitutions, thus suggesting only minimal changes in the functionality, if any at all; we could cite the convincing and relevant evidence reported by Radutoiu et al.27 that the amino-acid residue 118 of the second LysM module of NFR5 is essential for the recognition of rhizobia by species of Lotus japonicus and Lotus filicaulis. Our finding that the Mesoamerican-bean NFR5 has glutamine (Q) in position 151, whereas the Andean and the AHD both have proline (P)—neither of which amino acids is neutral—would merit further investigation to evaluate if such a mutation might play a role in nodulation preference. Although this result must be considered with caution, we found that the conserved polymorphism in the NFR1 and NFR5 proteins has caused the beans representative of the genetic pool Ecuador-Peru—i. e., the AHD—to be grouped in a cluster separate from those of Mesoamerica and the Andes. What we found to be interesting was that the phylogenetic and RMSD profiles of grouping the sequences are consistent with different evolutionary pathways in beans from the AHD and the Andean areas. This observation agrees with the proposal of Randón-Anaya et al.2 that those former beans from northern Peru-Ecuador originated from an ancestral form earlier than that of Mesoamerican- and Andean-bean genotypes. In addition, by applying a suppressive subtractive hybridization approach a set of bean genes were identified in our laboratory to be expressed in early step of infection by the cognate rhizobia28. Taken these results together, we conclude that genomic regions and patterns of expression in the host appear associated with an affinity for nodulation.Within a broader context, we believe that our results on the biogeography of bean-rhizobia interactions in the region where the origin and domestication of the host plants occurred provide novel useful issues to be considered in inoculation programs, for instance those involving selection of strains and cultivars, and invite to validate these findings in follow up field trials. More