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    Ecological niche model transferability of the white star apple (Chrysophyllum albidum G. Don) in the context of climate and global changes

    IPBES (2019): Summary for policymakers of the global assessment report on biodiversity and ecosystem services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services. S. Díaz, J. Settele, E. S. Brondízio E.S., H. T. Ngo, M. Guèze, J. Agard, A. Arneth, P. Balvanera, K. A. Brauman, S. H. M. Butchart, K. M. A. Chan, L. A. Garibaldi, K. Ichii, J. Liu, S. M. Subramanian, G. F. Midgley, P. Miloslavich, Z. Molnár, D. Obura, A. Pfaff, S. Polasky, A. Purvis, J. Razzaque, B. Reyers, R. Roy Chowdhury, Y. J. Shin, I. J. Visseren-Hamakers, K. J. Willis, and C. N. Zayas (eds.). IPBES secretariat, Bonn, Germany. 56 p.FAO. in Global Forest Resources Assessment 2020: Main report. Rome. https://doi.org/10.4060/ca9825en (2020).Millennium Ecosystem Assessment (MA). Ecosystems and Human Well-Being: Synthesis. Island Press, Washington (2005)CBD. Considerations for Implementing International Standards and Codes of Conduct in National Invasive Species. Strategies and Plans. CBD (2011).Semper-Pascual, A. et al. Using occupancy models to assess the direct and indirect impacts of agricultural expansion on species’ populations. Biodivers. Conserv. 29, 3669–3688 (2020).
    Google Scholar 
    IPCC. Provisional State of the Global Climate. 2022. https://storymaps.arcgis.com/stories/5417cd9148c248c0985a5b6d028b0277, Accessed 23rd December 2022.Nunez, S. & Alkemade, R. Exploring interaction effects from mechanisms between climate and land-use changes and the projected consequences on biodiversity. Biodivers. Conserv. 30, 3685–3696 (2021).
    Google Scholar 
    Liu, C., White, M. & Newell, G. Measuring and comparing the accuracy of species distribution models with presence absence data. Ecography 34, 232–243. https://doi.org/10.1111/j.1600-0587.2010.06354.x (2011).Article 
    CAS 

    Google Scholar 
    Hao, T., Elith, J., Lahoz-Monfort, J. J. & Guillera-Arroita, G. Testing whether ensemble modelling is advantageous for maximising predictive performance of species distribution models. Ecography 43, 549–558. https://doi.org/10.1111/ecog.04890 (2020).Article 

    Google Scholar 
    Pearson, G. R., Raxworthy, J. C., Nakamura, M. & Peterson, A. T. Predicting species distributions from small numbers of occurrence records: A test case using cryptic geckos in Madagascar. J. Biogeogr 34, 102–117 (2007).
    Google Scholar 
    Thuiller, W. et al. Niche-based modelling as a tool for predicting the risk of alien plant invasions at a global scale. Glob. Chang. Biol. 11, 2234–2250 (2005).ADS 

    Google Scholar 
    He, Y. et al. Predicting potential global distribution and risk regions for potato cyst nematodes (Globodera rostochiensis and Globodera pallida). Sci. Rep. 12(1), 1–10 (2022).ADS 
    CAS 

    Google Scholar 
    Elith, J., Kearney, M. & Phillips, S. The art of modelling range-shifting species. Methods Ecol. Evol. 1, 330–342 (2010).
    Google Scholar 
    Ashraf, U., Chaudhry, M. N. & Peterson, A. T. Ecological niche models of biotic interactions predict increasing pest risk to olive cultivars with changing climate. Ecosphere 12, e03714. https://doi.org/10.1002/ecs2.3714 (2021).Article 

    Google Scholar 
    Elith, J. et al. A statistical explanation of MaxEnt for ecologists. Divers. Distrib. 17, 43–57 (2011).
    Google Scholar 
    Ganglo, J. C. et al. Ecological niche modeling and strategies for the conservation of Dialium guineense Willd. (Black velvet) in West Africa. Int. J. Biodivers. Conserv. 9, 373–388 (2017).
    Google Scholar 
    Djotan, A. K. G. et al. How far can climate changes help to conserve and restore Garcinia kola Heckel, an extinct species in the wild in Benin (West Africa). Int. J. Biodivers. Conserv. 10, 203–213 (2018).
    Google Scholar 
    Kakpo, S. B. et al. Spatial distribution and impacts of climate change on Milicia excelsa in Benin, West Africa. J. For. Res. 32, 143–150. https://doi.org/10.1007/s11676-019-01069-7 (2021).Article 

    Google Scholar 
    Jung, M. et al. A global map of terrestrial habitat types. Sci. Data 7(1), 1–8 (2020).MathSciNet 

    Google Scholar 
    Poor, E. E., Scheick, B. K. & Mullinax, J. M. Multiscale consensus habitat modeling for landscape level conservation prioritization. Sci. Rep. 10(1), 1–13 (2020).
    Google Scholar 
    Schüßler, D., Mantilla-Contreras, J., Stadtmann, R., Ratsimbazafy, J. H. & Radespiel, U. Identification of crucial stepping stone habitats for biodiversity conservation in northeastern Madagascar using remote sensing and comparative predictive modeling. Biodivers. Conserv. 29, 2161–2184 (2020).
    Google Scholar 
    Campos-Cerqueira, M. et al. Climate change is creating a mismatch between protected areas and suitable habitats for frogs and birds in Puerto Rico. Biodivers. Conserv. 30, 3509–3528 (2021).
    Google Scholar 
    Biddle, R. et al. The value of local community knowledge in species distribution modelling for a threatened Neotropical parrot. Biodivers. Conserv. 30, 1803–1823 (2021).
    Google Scholar 
    Costa, A. et al. Modelling the amphibian chytrid fungus spread by connectivity analysis: Towards a national monitoring network in Italy. Biodivers. Conserv. 30(10), 2807–2825 (2021).
    Google Scholar 
    Konowalik, K. & Nosol, A. Evaluation metrics and validation of presence-only species distribution models based on distributional maps with varying coverage. Sci. Rep. 11(1), 1–15 (2021).
    Google Scholar 
    Borgelt, J., Sicacha-Parada, J., Skarpaas, O. & Verones, F. Native range estimates for red-listed vascular plants. Sci. Data 9(1), 1–12 (2022).
    Google Scholar 
    Brychkova, G. et al. Climate change and land-use change impacts on future availability of forage grass species for Ethiopian dairy systems. Sci. Rep. 12(1), 1–16 (2022).
    Google Scholar 
    Carrara, R. & Roig-Juñent, S. A. Maps of potential biodiversity: when the tools for regional conservation planning clash with species ecological niches. Biodivers. Conserv. 31(2), 651–665 (2022).
    Google Scholar 
    Critchlow, R. et al. Multi-taxa spatial conservation planning reveals similar priorities between taxa and improved protected area representation with climate change. Biodivers. Conserv. 31(2), 683–702 (2022).
    Google Scholar 
    González-Orozco, C. E., Porcel, M., Rodriguez-Medina, C. & Yockteng, R. Extreme climate refugia: A case study of wild relatives of cacao (Theobroma cacao) in Colombia. Biodivers. Conserv. 31(1), 161–182 (2022).
    Google Scholar 
    Karami, S., Ejtehadi, H., Moazzeni, H., Vaezi, J. & Behroozian, M. Minimal climate change impacts on the geographic distribution of Nepeta glomerulosa, medicinal species endemic to southwestern and central Asia. Sci. Rep. 12(1), 1–10 (2022).ADS 
    CAS 

    Google Scholar 
    Montemayor, S. I., Besteiro, S. I. & del Río, M. G. Integrating ecological and biogeographical tools for the identification of conservation areas in two Neotropical biogeographic provinces in Argentina based on phytophagous insects. Biodivers. Conserv. 31(7), 1969–1986 (2022).
    Google Scholar 
    da Silva, L. B. et al. How future climate change and deforestation can drastically affect the species of monkeys endemic to the eastern Amazon, and priorities for conservation. Biodivers. Conserv. 31(3), 971–988 (2022).
    Google Scholar 
    Yousefi, M. & Naderloo, R. Global habitat suitability modeling reveals insufficient habitat protection for mangrove crabs. Sci. Rep. 12(1), 1–9 (2022).
    Google Scholar 
    Yudaputra, A. et al. Habitat preferences, spatial distribution and current population status of endangered giant flower Amorphophallus titanum. Biodivers. Conserv. 31(3), 831–854 (2022).
    Google Scholar 
    Gomes, V. H. et al. Species distribution modelling: Contrasting presence-only models with plot abundance data. Sci. Rep. 8(1), 1–12 (2018).
    Google Scholar 
    Hoveka, L. N., van der Bank, M., Bezeng, B. S. & Davies, T. J. Identifying biodiversity knowledge gaps for conserving South Africa’s endemic flora. Biodivers. Conserv. 29, 2803–2819 (2020).
    Google Scholar 
    Macdonald, D. W. et al. Predicting biodiversity richness in rapidly changing landscapes: Climate, low human pressure or protection as salvation?. Biodivers. Conserv. 29, 4035–4057 (2020).
    Google Scholar 
    Peng, Y., Feng, J., Sang, W. & Axmacher, J. C. Geographical divergence of species richness and local homogenization of plant assemblages due to climate change in grasslands. Biodivers. Conserv. 31(3), 797–810 (2022).
    Google Scholar 
    Rincón, V. et al. Connectivity of Natura 2000 potential natural riparian habitats under climate change in the Northwest Iberian Peninsula: Implications for their conservation. Biodivers. Conserv. 31(2), 585–612 (2022).MathSciNet 

    Google Scholar 
    Leta, S. et al. Modeling the global distribution of Culicoides imicola: An Ensemble approach. Sci. Rep. 9(1), 1–9 (2019).ADS 
    CAS 

    Google Scholar 
    Messina, J. P. et al. The current and future global distribution and population at risk of dengue. Nat. Microbiol. 4(9), 1508–1515 (2019).CAS 

    Google Scholar 
    Redding, D. W. et al. Impacts of environmental and socio-economic factors on emergence and epidemic potential of Ebola in Africa. Nat. Commun. 10, 4531 (2019).ADS 

    Google Scholar 
    Klitting, R. et al. Predicting the evolution of the Lassa virus endemic area and population at risk over the next decades. Nat. Commun. 13(1), 1–15 (2022).
    Google Scholar 
    Li, Y. P., Gao, X., An, Q., Sun, Z. & Wang, H. B. Ecological niche modeling based on ensemble algorithms to predicting current and future potential distribution of African swine fever virus in China. Sci. Rep. 12(1), 1–11 (2022).ADS 

    Google Scholar 
    Oppel, S., Schaefer, H. M., Schmidt, V. & Schröder, B. How much suitable habitat is left for the last known population of the Pale-headed Brush-Finch?. The Condor 106, 429–434 (2004).
    Google Scholar 
    Heikkinen, R. K., Marmion, M. & Luoto, M. Does the interpolation accuracy of species distribution models come at the expense of transferability?. Ecography 35, 276–288 (2012).
    Google Scholar 
    Manzoor, S. A., Griffiths, G. & Lukac, M. Species distribution model transferability and model grain size–finer may not always be better. Sci. Rep. 8(1), 1–9 (2018).
    Google Scholar 
    Yates, K. L. et al. Outstanding challenges in the transferability of ecological models. Trends Ecol. Evol. 33, 790–802. https://doi.org/10.1016/j.tree.2018.08.001 (2018).Article 

    Google Scholar 
    Gantchoff, M. G. et al. Distribution model transferability for a wide-ranging species, the Gray Wolf. Sci. Rep. 12(1), 1–11 (2022).
    Google Scholar 
    Lyam, P. T., Adeyemi, T. O. & Ogundipe, O. T. Distribution modelling of Chrysophyllum albidum G. Don. in South-West Nigeria. J. Nat. Environ. Sci. 3, 7–14 (2012).
    Google Scholar 
    Orwa, C., Mutua, A., Kindt, R., Jamnadass, R., & Simons, A. Agroforestree Database: a tree reference and selection guide version 4.0. World Agroforestry Centre, Kenya. http://www.worldagroforestry.org/af/treedb/ (2009).Bolanle-Ojo, O. T. & Onyekwelu, J. C. Socio-economic importance of Chrysophyllum albidum G. Don. Rainforest and derived savanna ecosystems of Ondo state, Nigeria. Eur. J. Agric. For. Res. 2, 43–51 (2014).
    Google Scholar 
    Ugwu, J. A. & Umeh, V. C. Assessment of African star apple (Chrysophyllum albidum) fruit damage due to insect pests in Ibadan Southwest Nigeria. Res. J. For. 9, 87–92 (2015).
    Google Scholar 
    Akoegninou, A., Van der Burg, W. J. & Van der Maesen, L. J. G. in Flore Analytique du Bénin (No. 06.2). Backhuys Publishers. (2006).Houessou, L. G., Lougbegnon, T. O., Gbesso, F. G., Anagonou, L. E. & Sinsin, B. Ethno-botanical study of the African star apple (Chrysophyllum albidum G. Don) in the Southern Benin (West Africa). J. Ethnobiol. Ethnomed. 8, 1–10 (2012).
    Google Scholar 
    Lougbégnon, O. T., Nassi, K. M. & Gbesso, G. H. F. Ethnobotanique quantitative de l’usage de Chrysophyllum albidum G. Don par les populations locales au Bénin. J. Appl. Biosci. 95, 9028–9038 (2015).
    Google Scholar 
    Nartey, D., Gyesi, J. N., & Borquaye, L. S. Chemical composition and biological activities of the essential oils of Chrysophyllum albidum G. Don (African star apple). Biochem. Res. Int. 2021 (2021).Olajide, O., Udo, E. S., & Out, D. O. Diversity and population of timber tree species producing valuable non-timber products in two tropical rainforests in cross river state, Nigeria. J. Agric. Soc. Sci. ISSN Print 1813–2235 (2008)Platts, P. J., Omeny, P. & Marchant, R. AFRICLIM: High-resolution climate projections for ecological applications in Africa. Afr. J. Ecol. 53, 103–108 (2015).
    Google Scholar 
    Hajima, T. et al. Development of the MIROC-ES2L Earth system model and the evaluation of biogeochemical processes and feedbacks. Geosci. Model Dev. 13, 2197–2244 (2020).ADS 

    Google Scholar 
    Aiello-Lammens, M. E., Boria, R. A., Radosavljevic, A., Vilela, B. & Anderson, R. P. An R package for spatial thinning of species occurrence records for use in ecological niche models. Ecography 38, 541–545 (2015).
    Google Scholar 
    Lannuzel, G., Balmot, J., Dubos, N., Thibault, M. & Fogliani, B. High-resolution topographic variables accurately predict the distribution of rare plant species for conservation area selection in a narrow-endemism hotspot in New Caledonia. Biodivers. Conserv. 30, 963–990 (2021).
    Google Scholar 
    Scales, K. L. et al. Scale of inference: On the sensitivity of habitat models for wide-ranging marine predators to the resolution of environmental data. Ecography 40, 210–220 (2017).
    Google Scholar 
    Fick, S. E. & Hijmans, R. J. (2017) WorldClim 2: New 1km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37(12), 4302–4315 (2017).
    Google Scholar 
    Center for International Earth Science Information Network: CIESIN—Columbia University. 2021. Gridded Population of the World, Version 4 (GPWv4): Administrative Unit Center Points with Population Estimates, Revision 11. Palisades, NY: NASA Socioeconomic Data and Applications Center (SEDAC). Last Accessed 7th December, 2021. https://doi.org/10.7927/H4BC3WMT (2018)Eyring, V. et al. Overview of the coupled model intercomparison project phase 6 (CMIP6) experimental design and organization. Geosci. Model Dev. 9, 1937–1958. https://doi.org/10.5194/gmd-9-1937-2016 (2016).Article 
    ADS 

    Google Scholar 
    Dormann, C. F. et al. Collinearity: A review of methods to deal with it and a simulation study evaluating their performance. Ecography 36, 27–46 (2013).
    Google Scholar 
    Naimi, B. & Araújo, M. B. sdm: A reproducible and extensible R platform for species distribution modelling. Ecography 39, 368–375. https://doi.org/10.1111/ecog.01881 (2016).Article 

    Google Scholar 
    R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/ (2020)Phillips, S. J., Anderson, R. P. & Schapire, R. E. Maximum entropy modeling of species geographic distributions. Ecol. Model. 190, 231–259 (2006).
    Google Scholar 
    Elith, J., Leathwick, J. R. & Hastie, T. A working guide to boosted regression trees. J. Anim. Ecol. 77, 802–813 (2008).CAS 

    Google Scholar 
    Breiman, L. Random forests. Mach. Learn. 45, 5–32. https://doi.org/10.1023/A:1010933404324 (2001).Article 
    MATH 

    Google Scholar 
    Zheng, B. & Agresti, A. Summarizing the predictive power of a generalized linear model. Stat. Med. 19, 1771–1781 (2000).CAS 

    Google Scholar 
    Hastie, T. J. in Generalized Additive Models, Statistical models, 249–307 (Routledge, 2017).Friedman, J. H. Multivariate adaptive regression splines. Ann. Stat. 19, 1–67 (1991).MathSciNet 
    MATH 

    Google Scholar 
    Allouche, O., Tsoar, A. & Kadmon, R. Assessing the accuracy of species distribution models: Prevalence, kappa and the true skill statistic (TSS). J. Appl. Ecol. 43, 1223–1232 (2006).
    Google Scholar 
    Barbet-Massin, M., Jiguet, F., Albert, C. H. & Thuiller, W. Selecting pseudo-absences for species distribution models: How, where and how many?. Methods Ecol. Evol. 3, 327–338 (2012).
    Google Scholar 
    QGIS Development Team. QGIS geographic information system. Open Source Geospatial Foundation Project. http://qgis.osgeo.org (2021)Fandohan, B. et al. Women’s traditional knowledge, use value, and the contribution of tamarind (Tamarindus indica L.) to rural households’ cash income in Benin. Econ. Bot. 64, 248–259 (2010).
    Google Scholar 
    Gouwakinnou, G. N., Lykke, A. M., Assogbadjo, A. E. & Sinsin, B. Local knowledge, pattern and diversity of use of Sclerocarya birrea. J. Ethnobiol. Ethnomed. 7, 1–9 (2011).
    Google Scholar 
    O’Donnell, M. S. & Ignizio, D. A. Bioclimatic predictors for supporting ecological applications in the conterminous United States. US Geological Surv. Data Ser. 691, 4–9 (2012).
    Google Scholar 
    United Nations. 2022. World population projected to reach 9.8 billion in 2050, and 11.2 billion in 2100. https://www.un.org/en/desa/world-population-projected-reach-98-billion-2050-and-112-billion-2100, Accessed 25th December 2022 .Gbesso, F. H. G., Tente, B. H. A., Gouwakinnou, G. N. & Sinsin, B. A. Influence des changements climatiques sur la distribution géographique de Chrysophyllum albidum G. Don (Sapotaceae) au Benin. Int. J. Biol. Chem. Sci. 7, 2007–2018 (2013).
    Google Scholar 
    Elith, J. et al. Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29, 129–151 (2006).
    Google Scholar 
    Mi, C., Huettmann, F., Guo, Y., Han, X. & Wen, L. Why choose random forest to predict rare species distribution with few samples in large undersampled areas? Three Asian crane species models provide supporting evidence. Peer J. 5, e2849. https://doi.org/10.7717/peerj.2849 (2017).Article 

    Google Scholar 
    Segurado, P. & Araujo, M. B. An evaluation of methods for modelling species distributions. J. Biogeogr. 31, 1555–1568 (2004).
    Google Scholar 
    Pearson, R. G. et al. Model-based uncertainty in species range prediction. J. Biogeogr. 33, 1704–1711 (2006).
    Google Scholar 
    Dambros, C. et al. The role of environmental filtering, geographic distance and dispersal barriers in shaping the turnover of plant and animal species in Amazonia. Biodivers. Conserv. 29, 3609–3634 (2020).
    Google Scholar  More

  • in

    Genomic architecture of migration timing in a long-distance migratory songbird

    Davidson, S. C. et al. Ecological insights from three decades of animal movement tracking across a changing arctic. Science 370, 712–715 (2020).ADS 
    CAS 

    Google Scholar 
    Cohen, J. M., Lajeunesse, M. J. & Rohr, J. R. A global synthesis of animal phenological responses to climate change. Nat. Clim. Chang. 8, 224–228 (2018).ADS 

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

    Google Scholar 
    Studds, C. E. & Marra, P. P. Rainfall-induced changes in food availability modify the spring departure programme of a migratory bird. Proc. R. Sci. B. 278, 3437–3443 (2011).
    Google Scholar 
    González, A. M., Bayly, N. J. & Hobson, K. A. Earlier and slower or later and faster: spring migration pace linked to departure time in a Neotropical migrant songbird. J. Anim. Ecol. 89, 2840–2851 (2020).
    Google Scholar 
    Liedvogel, M., Åkesson, S. & Bensch, S. The genetics of migration on the move. Trends Ecol. Evol. 26, 561–569 (2011).
    Google Scholar 
    Caprioli, M. et al. Clock gene variation is associated with breeding phenology and maybe under directional selection in the migratory barn swallow. PLoS ONE 7, e35140 (2012).ADS 
    CAS 

    Google Scholar 
    Mettler, R., Segelbacher, G. & Schaefer, M. H. Interactions between a candidate gene for migration (ADCYAP1), morphology and sex predict spring arrival in blackcap populations. PLoS ONE 10, e0144587 (2015).
    Google Scholar 
    Bazzi, G. et al. Clock gene polymorphism and scheduling of migration: a geolocator study of the barn swallow Hirundo rustica. Sci. Rep. 5, 12443 (2015).ADS 

    Google Scholar 
    Saino, N. et al. Polymorphism at the Clock gene predicts phenology of long-distance migratoin in birds. Mol. Ecol. 24, 1758–1773 (2015).CAS 

    Google Scholar 
    Bossu, C. M. et al. Clock-linked genes underlie seasonal migratory timing in a diurnal raptor. Proc. R. Soc. B. 289, 20212507 (2022).CAS 

    Google Scholar 
    O’Malley, K. G., Ford, M. J. & Hard, J. J. Clock polymorphism in Pacific salmon: evidence for variable selection along a latitudinal gradient. Proc. R. Soc. B. 277, 3703–3714 (2010).
    Google Scholar 
    Peterson, M. P. et al. Variation in candidate genes CLOCK and ADCYAP1 does not consistently predict differences in migratory behavior in the songbird genus Junco. F1000Research 2 (2013).McKinnon, E. A. & Ten Love, O. P. years tracking the migrations of small landbirds: Lessons learned in the golden age of bio-logging. Auk 135, 834–856 (2018).
    Google Scholar 
    Fraser, K. C. et al. Continent-wide tracking to determine migratory connectivity and tropical habitat associations of a declining aerial insectivore. Proc. R. Soc. B. 279, 4901–4906 (2012).
    Google Scholar 
    Neufeld, L. R. et al. Breeding latitude is associated with the timing of nesting and migration around the annual calendar among purple martin Progne subis populations. J. Ornithol. 162, 1009–1024 (2021).
    Google Scholar 
    Peona, V. et al. Identifying the causes and consequences of assembly gaps using a multiplatform genome assembly of a bird-of-paradise. Mol. Ecol. 21(1), 263–286 (2020).
    Google Scholar 
    Coelho, L. A., Musher, L. J. & Cracraft, J. A multireference-based whole genome assembly for the obligate ant-following antbird, Rhegmatorhina melanosticta (Thamnophilidae). Diversity 11(19), 144 (2019).CAS 

    Google Scholar 
    Zhou, X., Carbonetto, P. & Stephens, M. Polygenic modeling with Bayesian sparse linear mixed models. PLoS Genet. 9, e1003264 (2013).CAS 

    Google Scholar 
    Fuller, Z. L. et al. Population genetics of the coral Acropora millepora: Towards a genomic predictor of bleaching. Science 369(6501) (2019).Jones, S., Pfister-Genskow, M., Benca, R. M. & Cirelli, C. Molecular correlates of sleep and wakefulness in the brain of the white-crowned sparrow. J. Neurochem. 105, 46–62 (2008).CAS 

    Google Scholar 
    Ma, C. et al. Sleep regulation by neurotensinergic neurons in a thalamo-amygdala circuit. Neuron 103 (2019).Wong, J. M. & Eirin-Lopez, J. M. Evolution of methyltransferase-like (METTL) proteins in metazoan: a complex gene family involved in epitranscriptomic regulation and other epigenetic processes. Mol. Biol. Evol. 38, 5309–5327 (2021).CAS 

    Google Scholar 
    Jia, Z. et al. ACSS3 in brown fast drives propionate catabolism and its deficiency leads to autophagy and systemic metabolic dysfunction. Clin. Transl. Med. 12, e665 (2022).CAS 

    Google Scholar 
    Muller, F. et al. Towards a conceptual framework for explaining variation in nocturnal departure time of songbird migrants. Mov. Ecol. 4, 24 (2016).
    Google Scholar 
    Fraser, K. C. et al. Individual variability in migration timing can explain long-term population-level advances in a songbird. Front. Ecol. Evol. 7, 324 (2019).ADS 

    Google Scholar 
    Barret, R. D. H. & Schluter, D. Adaptation from standing genetic variation. Trends Ecol. Evol. 23(1), 38–44 (2008).
    Google Scholar 
    Colodro-Conde, L. et al. A direct test of the diathesis-stress model for depression. Mol. Psychiatry 23, 1590–1596 (2017).
    Google Scholar 
    Dudbridge, F. Power and predictive accuracy of polygenic risk scores. PLOS Genetics 9(4) (2013).Lavallée, C. D. et al. The use of nocturnal flights for barrier crossing in a diurnally migrating songbird. Mov. Ecol. 9, 21 (2021).
    Google Scholar 
    Saino, N. et al. Migration phenology and breeding success are predicted by methylation of a photoperiodic gene in the barn swallow. Sci. Rep. 7, 45412 (2017).ADS 
    CAS 

    Google Scholar 
    Henry, R. A. et al. Changing the selectivity of p300 by acetyl-CoA modulation of histone acetylation. ACS Chem. Biol 10, 146–156 (2015).CAS 

    Google Scholar 
    Sun, H., Skorgerbø, G., Wang, Z., Liu, W. & Li, Y. Structural relationships between highly conserved elements and genes in vertebrate genomes. PLoS ONE 3, e3727 (2008).ADS 

    Google Scholar 
    Chin, C. S. et al. Phased diploid genome assembly with single-molecule real-time sequencing. Nat. Methods 13, 1050–1054 (2016).CAS 

    Google Scholar 
    Chin, C. S. et al. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat. Methods 10, 563–569 (2013).CAS 

    Google Scholar 
    Koren, S. et al. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res. 27, 722–736 (2017).CAS 

    Google Scholar 
    Walker, B. J. et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 9, e112963 (2014).ADS 

    Google Scholar 
    Coombe, L. et al. ARKS: Chromosome-scale scaffolding of human genome drafts with linked read kmers. BMC Bioinform. 19, 1–10 (2018).
    Google Scholar 
    Campbell, M. S., Holt, C., Moore, B. & Yandell, M. Genome annotation and curation using MAKER and MAKER‐P. Curr. Protocols Bioinform. 48, 4.11.1–4.11.39 (2014).Malmberg, M. M. et al. Evaluation and recommendations for routine genotyping using skim whole genome re-sequencing in canola. Front. Plant. Sci. 9 (2018).Browning, B. L. & Browning, S. R. Genotype imputation with millions of reference samples. Am. J. Hum. Genet. 98, 116–126 (2016).CAS 

    Google Scholar 
    Golicz, A. A., Bayer, P. E. & Edwards, D. Skim-based genotyping by sequencing. Methods Mol. Biol. 1245, 257–270 (2015).CAS 

    Google Scholar 
    Hill, R. D. Theory of geolocation by light levels. In B. J. L. Boeuf, & R. M. Laws (Ed.), Elephant seals: Population ecology, behaviour and physiology, pp. 227–236. Berkeley, CA: University of California Press (1994).Wotherspoon, S., Summer, M. & Lisovski, S. BAStag: basic data processing for light based geolocation archival tags. Version 0.1.3. (2016).Lisovski, S. & Hahn, S. GeoLight-processing and anslysing light-based geolocator data in R. Methods Ecol. Evol. 3, 1055–1059 (2012).
    Google Scholar 
    Gompert, Z., Lucas, L. K., Nice, C. C. & Buerkle, C. A. Genome divergence and the genetic architecture of barriers to gene flow between Lycaeides idas and L. melissa. Evolution 67, 2498–2514 (2013).
    Google Scholar 
    Pfeifer, S. P. et al. The evolutionary history of Nebraska deer mice: local adaptation in the face of strong gene flow. Mol. Biol. Evol. 35, 792–806 (2018).CAS 

    Google Scholar 
    Purcell, S. et al. PLINK: a toolset for whole-genome association and population-based linkage analysis. Am. J. Hum. Genet. 81, 559–575 (2007).CAS 

    Google Scholar 
    Choi, S. W., Mak, T. S. & O’Reilly, P. F. Tutorial: a guide to performing polygenic risk score analysis. Nat Protoc 15, 2759–2772 (2020).CAS 

    Google Scholar 
    Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158 (2011).CAS 

    Google Scholar 
    Cruickshank, T. E. & Hahn, M. W. Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow. Mol. Ecol. 23, 3133–3157 (2014).
    Google Scholar 
    Vijay, N. et al. Evolution of heterogeneous genome differentiation across multiple contact zones in a crow species complex. Nat. Commun. 7, 13195 (2016).ADS 
    CAS 

    Google Scholar 
    Delmore, K. et al. The evolutionary history and genomics of European blackcap migration. eLife 9, e54462 (2020). More

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    Mangrove reforestation provides greater blue carbon benefit than afforestation for mitigating global climate change

    Literature search and screeningOur analysis included a systematic literature search and was conducted by following the PRISMA protocol55 (Supplementary Fig. 7). We searched through Web of Science and China National Knowledge Infrastructure (CNKI) platforms by using keywords listed in Supplementary Table 3. A total of 3299 potentially relevant articles were found (Mandarin and English). The availability of peer-reviewed datasets associated with these published articles11,15,56,57,58,59 and online databases (The Sustainable Wetlands Adaptation and Mitigation Program (SWAMP) database, https://www2.cifor.org/swamp) were also considered. We then removed a significant number of articles through title screening, leaving 551 articles for further inspection.For these remaining articles, we used a four-step critique process to screen their title, abstract, and full text. We determined that firstly, they must provide carbon density data for at least one of the four mangrove carbon pools (i.e., aboveground biomass, belowground biomass, sediment organic carbon, or total ecosystem carbon). Secondly, articles needed to state the forest age or the starting date of the restoration action. For those studies providing only age intervals (e.g., 10–25 years, >66 years), we excluded them from the analysis. Thirdly, a description of prior land use was required. From these, mangrove restoration could be divided into two categories—reforestation and afforestation—on whether mangroves previously existed in that location. For reforestation, the initial conditions for inclusion were: (1) abandoned agricultural/aquacultural sites built previously by excavating mangrove forests, (2) clear-felled mangrove lands after wars, timber harvest, and silvicultural management, and (3) mangrove forests with mortality due to spraying of defoliants and hydrological alteration caused by the construction of embankments. We compared the carbon densities of reforested mangroves among sites with different causes of degradation/deforestation, and no significant difference is found (Supplementary Fig. 9). For those reforested mangroves, we assumed they would be protected and conserved by local governments and non-government organizations, so that there will not be human-driven degradation or deforestation in the near future. However, we acknowledge that a fraction of mangrove reforestation is managed for wood production, which means logging would happen at a certain interval after reforestation at these sites. For these logging sites, we used their reported measurements after clear-cut, such as 0-, 5-, 10-, 15-, and 25-year post-harvest sites in Sundarbans, Bangladesh60. On the other hand, the future occurrence of natural-driven deforestation (e.g., cyclones) is difficult to predict, and thus not considered in our study. For afforestation, the initial condition for inclusion was the presence of non-mangrove habitat immediately before afforestation began, such as mudflats, seagrass, saltmarsh, coral reef, or denuded areas. In most cases, reforestation and afforestation were undertaken through active planting without much re-engineering4, but for reforestation, natural regeneration could have, and in many places likely did, augment recruitment61. Moreover, we only considered mangrove succession that started from near-barren land with an insignificant amount of biomass, and introductions of exotic species to degraded areas with sparse trees were not incorporated. Lastly, if the forest age or prior land use type was not given, the articles needed to specify the location of sampling plots (latitude, longitude). With the coordinates matching, prior land use type and establishment dates were sometimes identifiable through remote sensing (Supplementary Fig. 10). For those articles sharing the same restoration sites but showing different aspects of the data collection, we combined the results and considered the collective work as one source. Based on the space-for-time method, data in the control sites before mangrove restoration actions were also collected as a paired site of restoration (e.g., abandoned ponds before mangrove reforestation; mudflats before mangrove afforestation). In total, we obtained data from 379 mangrove restoration sites described by 106 articles.Data extractionWe extracted aboveground living biomass carbon (AGC), belowground living biomass carbon (BGC), sediment carbon (SCS), and total ecosystem carbon (TECS) density from the 106 original data sources. In most cases, numeric values were provided. For those data not provided numerically but graphed, we determined values from figures with the application of GetData Graph Digitizer (http://getdata-graph-digitizer.com/).Among the articles, aboveground and belowground biomass (Mg ha−1) data were obtained using either a harvesting method (empirical) or an allometric method (calculation). Aboveground biomass represented the sum of stem, leaf, and branch dry weight, and we included prop root biomass when Rhizophora spp. were present. For soil coring methods that determined belowground biomass or sediment carbon density, belowground biomass was considered the dry weight of living coarse and fine roots multiplied by the ratio of core area to land surface area62. For allometric methods, trunk diameter at breast height (DBH, ~1.3 m) and tree height were used to calculate aboveground and belowground biomass by species-specific or common allometric equations63. These equations were also used to calculate the belowground biomass when articles provided plot information (DBH, height) but not belowground biomass (Supplementary Table 4). Total biomass was calculated as the sum of aboveground and belowground biomass. Deadwood and pneumatophore biomass were not included in our analysis; these data are rarely provided and/or methods of determination are inconsistent among global studies64. Some articles provided total biomass and shoot/root biomass ratio (S/R), and in such cases, above- and belowground biomass data were obtained through calculation as follows:$${{{{{rm{Aboveground}}}}}},{{{{{rm{biomass}}}}}}={{{{{rm{Total}}}}}},{{{{{rm{biomass}}}}}}times frac{frac{S}{R}}{frac{S}{R}+1}$$
    (1)
    $${{{{{rm{Belowground}}}}}},{{{{{rm{biomass}}}}}}={{{{{rm{Total}}}}}},{{{{{rm{biomass}}}}}}times frac{1}{frac{S}{R}+1}$$
    (2)
    For those articles measuring carbon content, study-specific carbon conversion factors were used to transform biomass to biomass carbon density (Mg C ha−1). If carbon content data were not provided, we converted aboveground and belowground biomass to carbon density by applying a conversion of 0.47 and 0.39, respectively65. The aboveground biomass carbon density was divided by its corresponding age to get the average aboveground biomass carbon accumulation rate (Mg C ha−1 yr−1).For sediment carbon density (SCS, Mg C ha−1), we selected the top 1 m because this depth equated to the most commonly reported depth and could reflect the impact of root mass input in the deeper depth66, which is also consistent with recent blue carbon standing stock assessment guidance64,67. Sediment carbon stock was calculated by multiplying sediment organic carbon content (SOC, %) by bulk density (BD, g cm−3), integrated over depth (cm). For studies that reported sediment carbon stock to More

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    Family before work: task reversion in workers of the red imported fire ant, Solenopsis invicta in the presence of brood

    Wilson, E. O. The Insect Societies (Oxford University Press, 1971).
    Google Scholar 
    Beshers, S. N. & Fewell, J. H. Models of division of labor in social insects. Annu. Rev. Entomol. 46, 413–440 (2001).CAS 

    Google Scholar 
    Seeley, T. D. Adaptive significance of the age polyethism schedule in honeybee colonies. Behav. Ecol. Sociobiol. 4, 287–293 (1982).
    Google Scholar 
    Tallamy, D. W. Insect parental care. Bioscience 34, 20–24. https://doi.org/10.2307/1309421 (1984).Article 

    Google Scholar 
    Queller, D. C. Extended parental care and the origin of eusociality. Proc. R. Soc. Lond. Ser. B: Biol. Sci. 256, 105–111. https://doi.org/10.1098/rspb.1994.0056 (1994).Article 
    ADS 

    Google Scholar 
    Bigley, W. S. & Vinson, S. B. Characterization of a brood pheromone isolated from the sexual brood of the imported fire ant, Solenopsis invicta 1,2. Ann. Entomol. Soc. Am. 68, 301–304 (1975).CAS 

    Google Scholar 
    Endler, A. et al. Surface hydrocarbons of queen eggs regulate worker reproduction in a social insect. Proc. Natl. Acad. Sci. USA 101, 2945–2950. https://doi.org/10.1073/pnas.0308447101 (2004).Article 
    ADS 
    CAS 

    Google Scholar 
    Maisonnasse, A., Lenoir, J. C., Beslay, D., Crauser, D. & Le Conte, Y. E-beta-ocimene, a volatile brood pheromone involved in social regulation in the honey bee colony (Apis mellifera). PLoS ONE 5, e13531. https://doi.org/10.1371/journal.pone.0013531 (2010).Article 
    ADS 
    CAS 

    Google Scholar 
    Schultner, E., Oettler, J. & Helantera, H. The role of brood in eusocial hymenoptera. Q. Rev. Biol. 92, 39–78. https://doi.org/10.1086/690840 (2017).Article 

    Google Scholar 
    Amdam, G. V., Hartfelder, K., Norberg, K., Hagen, A. & Omholt, S. W. Altered physiology in worker honey bees (Hymenoptera: Apidae) infested with the mite Varroa destructor (Acari: Varroidae): A factor in colony loss during overwintering? J. Econ. Entomol. 97, 741–747 (2004).
    Google Scholar 
    Calabi, P. & Traniello, J. F. Behavioral flexibility in age castes of the ant Pheidole dentata. J. Insect Behav. 2, 663–677 (1989).
    Google Scholar 
    Gordon, D. W. Dynamics of task switching in harvester ants. Anim. Behav. 38, 194–204 (1989).
    Google Scholar 
    Robinson, G. E. Regulation of division of labor in insect societies. Annu. Rev. Entomol. 37, 637–665. https://doi.org/10.1146/annurev.en.37.010192.003225 (1992).Article 
    CAS 

    Google Scholar 
    Robinson, E. J., Feinerman, O. & Franks, N. R. Flexible task allocation and the organization of work in ants. Proc. R. Soc. B: Biol. Sci. 276, 4373–4380 (2009).
    Google Scholar 
    Nijhout, H. F. & Wheeler, D. E. Juvenile-hormone and the physiological-basis of Insect polymorphisms. Q. Rev. Biol. 57, 109–133. https://doi.org/10.1086/412671 (1982).Article 
    CAS 

    Google Scholar 
    Herb, B. R. et al. Reversible switching between epigenetic states in honeybee behavioral subcastes. Nat. Neurosci. 15, 1371–1373. https://doi.org/10.1038/nn.3218 (2012).Article 
    CAS 

    Google Scholar 
    Kensuke, N. Age polyethism, idiosyncrasy and behavioural flexibility in the queenless ponerine ant, Diacamma sp. J. Ethol. 13, 113–123 (1995).
    Google Scholar 
    Kensuke, N. Does behavioral flexibility compensate or constrain colony productivity? Relationship among age structure, labor allocation, and production of workers in ant colonies. J. Insect Behav. 9, 557–569 (1996).
    Google Scholar 
    Shimoji, H., Kasutani, N., Ogawa, S. & Hojo, M. K. Worker propensity affects flexible task reversion in an ant. Behav. Ecol. 74, 1–8 (2020).
    Google Scholar 
    Bernadou, A., Busch, J. & Heinze, J. Diversity in identity: Behavioral flexibility, dominance, and age polyethism in a clonal ant. Behav. Ecol. Sociobiol. 69, 1365–1375 (2015).
    Google Scholar 
    Kohlmeier, P., Feldmeyer, B. & Foitzik, S. Vitellogenin-like A—Associated shifts in social cue responsiveness regulate behavioral task specialization in an ant. PLoS Biol. 16, e2005747 (2018).
    Google Scholar 
    Tripet, F. & Nonacs, P. Foraging for work and age-based polyethism: The roles of age and previous experience on task choice in ants. Ethology 110, 863–877 (2004).
    Google Scholar 
    Kohlmeier, P., Alleman, A. R., Libbrecht, R., Foitzik, S. & Feldmeyer, B. Gene expression is more strongly associated with behavioural specialisation than with age or fertility in ant workers. Mol. Ecol. https://doi.org/10.1111/mec.14971 (2018).Article 

    Google Scholar 
    Levenbook, L. & Bauer, A. C. The fate of the larval storage protein calliphorin during adult development of Calliphora vicina. Insect Biochem. 14, 77–86 (1984).CAS 

    Google Scholar 
    Zhou, X., Oi, F. M. & Scharf, M. E. Social exploitation of hexamerin: RNAi reveals a major caste-regulatory factor in termites. Proc. Natl. Acad. Sci. 103, 4499–4504 (2006).ADS 
    CAS 

    Google Scholar 
    Zhou, X., Tarver, M. R., Bennett, G., Oi, F. & Scharf, M. Two hexamerin genes from the termite Reticulitermes flavipes: Sequence, expression, and proposed functions in caste regulation. Gene 376, 47–58 (2006).CAS 

    Google Scholar 
    Hawkings, C., Calkins, T. L., Pietrantonio, P. V. & Tamborindeguy, C. Caste-based differential transcriptional expression of hexamerins in response to a juvenile hormone analog in the red imported fire ant (Solenopsis invicta). PLoS ONE 14, e0216800 (2019).CAS 

    Google Scholar 
    Hoffman, E. A. & Goodisman, M. A. Gene expression and the evolution of phenotypic diversity in social wasps. BMC Biol. 5, 1–9 (2007).
    Google Scholar 
    Hunt, J. H., Buck, N. A. & Wheeler, D. E. Storage proteins in vespid wasps: Characterization, developmental pattern, and occurrence in adults. J. Insect Physiol. 49, 785–794 (2003).CAS 

    Google Scholar 
    Colgan, T. J. et al. Polyphenism in social insects: Insights from a transcriptome-wide analysis of gene expression in the life stages of the key pollinator, Bombus terrestris. BMC Genom. 12, 1–20 (2011).
    Google Scholar 
    Cremer, S., Armitage, S. A. & Schmid-Hempel, P. Social immunity. Curr. Biol. 17, R693–R702 (2007).CAS 

    Google Scholar 
    Cremer, S., Pull, C. D. & Fuerst, M. A. Social immunity: Emergence and evolution of colony-level disease protection. Annu. Rev. Entomol. 63, 105–123 (2018).CAS 

    Google Scholar 
    Danihlík, J., Aronstein, K. & Petřivalský, M. Antimicrobial peptides: A key component of honey bee innate immunity: Physiology, biochemistry, and chemical ecology. J. Apic. Res. 54, 123–136 (2015).
    Google Scholar 
    Koch, S. I. et al. Caste-specific expression patterns of immune response and chemosensory related genes in the leaf-cutting ant, Atta vollenweideri. PLoS ONE 8, e81518 (2013).ADS 

    Google Scholar 
    Chardonnet, F. et al. Food searching behaviour of a Lepidoptera pest species is modulated by the foraging gene polymorphism. J. Exp. Biol. 217, 3465–3473 (2014).
    Google Scholar 
    Scheiner, R., Page, R. E. Jr. & Erber, J. Responsiveness to sucrose affects tactile and olfactory learning in preforaging honey bees of two genetic strains. Behav. Brain Res. 120, 67–73 (2001).CAS 

    Google Scholar 
    Wang, Z. et al. Visual pattern memory requires foraging function in the central complex of Drosophila. Learn. Mem. 15, 133–142 (2008).
    Google Scholar 
    Zhou, Y., Lei, Y., Lu, L. & He, Y. Temperature-and food-dependent foraging gene expression in foragers of the red imported fire ant Solenopsis invicta Buren (Hymenoptera: Formicidae). Physiol. Entomol. 45, 1–6 (2020).
    Google Scholar 
    Ingram, K. K. et al. Context-dependent expression of the foraging gene in field colonies of ants: The interacting roles of age, environment and task. Proc. R. Soc. B: Biol. Sci. 283, 20160841 (2016).
    Google Scholar 
    Ingram, K. K., Oefner, P. & Gordon, D. M. Task-specific expression of the foraging gene in harvester ants. Mol. Ecol. 14, 813–818 (2005).CAS 

    Google Scholar 
    Lucas, C. & Sokolowski, M. B. Molecular basis for changes in behavioral state in ant social behaviors. Proc. Natl. Acad. Sci. 106, 6351–6356 (2009).ADS 
    CAS 

    Google Scholar 
    Ben-Shahar, Y. The foraging gene, behavioral plasticity, and honeybee division of labor. J. Comp. Physiol. A. 191, 987–994 (2005).CAS 

    Google Scholar 
    Daugherty, T., Toth, A. & Robinson, G. Nutrition and division of labor: Effects on foraging and brain gene expression in the paper wasp Polistes metricus. Mol. Ecol. 20, 5337–5347 (2011).CAS 

    Google Scholar 
    Morrison, L. W., Porter, S. D., Daniels, E. & Korzukhin, M. D. Potential global range expansion of the invasive fire ant, Solenopsis invicta. Biol. Invasions 6, 183–191 (2004).
    Google Scholar 
    Valles, S. M., Wetterer, J. K. & Porter, S. D. The red imported fire ant (Hymenoptera: Formicidae) in the West Indies: Distribution of natural enemies and a possible test bed for release of self-sustaining biocontrol agents. Fls. Entomol. 98, 1101–1105 (2015).
    Google Scholar 
    Greenberg, L., Vinson, S. & Ellison, S. Nine-year study of a field containing both monogyne and polygyne red imported fire ants (Hymenoptera: Formicidae). Ann. Entomol. Soc. Am. 85, 686–695 (1992).
    Google Scholar 
    Keller, L. & Ross, K. G. Selfish genes: A green beard in the red fire ant. Nature 394, 573–575 (1998).ADS 
    CAS 

    Google Scholar 
    Vinson, S. B. Impact of the invasion of the imported fire ant. Insect Sci. 20, 439–455 (2013).
    Google Scholar 
    Tschinkel, W. R. The Fire Ants (Harvard University Press, 2006).
    Google Scholar 
    Cassill, D. L. & Tschinkel, W. R. Task selection by workers of the fire ant Solenopsis invicta. Behav. Ecol. Sociobiol. 45, 301–310 (1999).
    Google Scholar 
    Mirenda, J. T. & Vinson, S. B. Division of labour and specification of castes in the red imported fire ant Solenopsis invicta Buren. Anim. Behav. 29, 410–420 (1981).
    Google Scholar 
    Wilson, E. O. Division of labor in fire ants based on physical castes (Hymenoptera: Formicidae: Solenopsis). J. Kansas Entomol. Soc. 51, 615–636 (1978).
    Google Scholar 
    Sorensen, A., Busch, T. M. & Vinson, S. B. Behavioral flexibility of temporal subcastes in the fire ant, Solenopsis invicta in response to food. Psyche 91, 319–331 (1984).
    Google Scholar 
    Bigley, W. S. & Vinson, S. B. Characterization of a brood pheromone isolated from the sexual brood of the imported fire ant, Solenopsis invicta. Ann. Entomol. Soc. Am. 2, 301–304 (1975).
    Google Scholar 
    Bajracharya, P., Lu, H. L. & Pietrantonio, P. V. The red imported fire ant (Solenopsis invicta Buren) kept Y not F: Predicted sNPY endogenous ligands deorphanize the short NPF (sNPF) receptor. PLoS ONE 9(10), e109590 (2014).ADS 

    Google Scholar 
    Castillo, P. Short neuropeptide F receptor in the worker brain of the red imported fire ant (Solenopsis invicta Buren) and methodology for RNA interference M.S. thesis, Texas A&M University (2015).Castillo, P. & Pietrantonio, P. V. Differences in sNPF receptor-expressing neurons in brains of fire ant (Solenopsis invicta Buren) worker subcastes: Indicators for division of labor and nutritional status? PLoS ONE 8, e83966 (2013).ADS 

    Google Scholar 
    Cassill, D. L. & Tschinkel, W. R. Allocation of liquid food to larvae via trophallaxis in colonies of the fire ant, Solenopsis invicta. Anim. Behav. 3, 801–813 (1995).
    Google Scholar 
    Cassill, D. L., Stuy, A. & Buck, R. G. Emergent properties of food distribution among fire ant larvae. J. Theor. Biol. 3, 371–381 (1998).ADS 

    Google Scholar 
    Dussutour, A. & Simpson, S. J. Communal nutrition in ants. Curr. Biol. 19, 740–744. https://doi.org/10.1016/j.cub.2009.03.015 (2009).Article 
    CAS 

    Google Scholar 
    Petralia, R. S. & Vinson, S. B. Feeding in the larvae of the imported fire ant, Solenopsis invicta: Behavior and morphological adaptations. Ann. Entomol. Soc. Am. 71, 643–648 (1978).
    Google Scholar 
    Petralia, R. S. & Vinson, S. B. Developmental morphology of larvae and eggs of the imported fire ant, Solenopsis invicta. Ann. Entomol. Soc. Am. 72, 472–484 (1979).
    Google Scholar 
    Chen, J. Advancement on techniques for the separation and maintenance of the red imported fire ant colonies. Insect Sci. 14, 1–4 (2007).
    Google Scholar 
    Banks, W. A. et al. (Agricultural Research (Southern Region), Science and Education…, 1981).Valles, S. M. & Porter, S. D. Identification of polygyne and monogyne fire ant colonies (Solenopsis invicta) by multiplex PCR of Gp-9 alleles. Insectes Soc. 2, 199–200 (2003).
    Google Scholar 
    Schmittgen, T. D. & Livak, K. J. Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3, 1101 (2008).CAS 

    Google Scholar 
    Cheng, D., Zhang, Z., He, X. & Liang, G. Validation of reference genes in Solenopsis invicta in different developmental stages, castes and tissues. PLoS ONE 8, e57718. https://doi.org/10.1371/journal.pone.0057718 (2013).Article 
    ADS 
    CAS 

    Google Scholar 
    Qiu, H.-L., Zhao, C.-Y. & He, Y.-R. On the molecular basis of division of labor in Solenopsis invicta (Hymenoptera: Formicidae) workers: RNA-seq analysis. J. Insect Sci. 17, 48 (2017).
    Google Scholar 
    Chen, J. et al. Role of the foraging gene in worker behavioral transition in the red imported fire ant, Solenopsis invicta (Hymenoptera: Formicidae). Pest Manag. Sci. https://doi.org/10.1002/ps.6921 (2022).Article 

    Google Scholar 
    Shorter, J. R. & Tibbetts, E. A. The effect of juvenile hormone on temporal polyethism in the paper wasp Polistes dominulus. Insectes Soc. 56, 7–13 (2009).
    Google Scholar 
    Pankiw, T., Page, R. E. Jr. & Kim Fondrk, M. Brood pheromone stimulates pollen foraging in honey bees (Apis mellifera). Behav. Ecol. Sociobiol. 44, 193–198. https://doi.org/10.1007/s002650050531 (1998).Article 

    Google Scholar 
    Smedal, B., Brynem, M., Kreibich, C. D. & Amdam, G. V. Brood pheromone suppresses physiology of extreme longevity in honeybees (Apis mellifera). J. Exp. Biol. 212, 3795–3801. https://doi.org/10.1242/jeb.035063 (2009).Article 
    CAS 

    Google Scholar 
    Solis, C. R. & Strassmann, J. E. Presence of brood affects caste differentiation in the social wasp, Polistes exclamans Viereck (Hymenoptera, Vespidae). Funct. Ecol. 4, 531–541. https://doi.org/10.2307/2389321 (1990).Article 

    Google Scholar 
    Traynor, K. S. Decoding Brood Pheromone: The Releaser and Primer Effects of Young and Old Larvae on Honey Bee (Apis mellifera) Workers (Arizona State University, 2014).
    Google Scholar 
    Wagoner, K. M., Spivak, M. & Rueppell, O. Brood affects hygienic behavior in the honey bee (Hymenoptera: Apidae). J. Econ. Entomol. 111, 2520–2530. https://doi.org/10.1093/jee/toy266 (2018).Article 
    CAS 

    Google Scholar 
    Nijhout, H. F. & Wheeler, D. E. Juvenile hormone and the physiological basis of insect polymorphisms. Q. Rev. Biol. 57, 109–133 (1982).CAS 

    Google Scholar  More

  • in

    Asynchrony in coral community structure contributes to reef-scale community stability

    Parmesan, C. Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 37, 637–669 (2006).
    Google Scholar 
    Elahi, R. et al. Recent trends in local-scale marine biodiversity reflect community structure and human impacts. Curr. Biol. 25, 1938–1943 (2015).CAS 

    Google Scholar 
    Harley, C. D. G. Climate change, keystone predation, and biodiversity loss. Science 334, 1124–1127 (2011).ADS 
    CAS 

    Google Scholar 
    Poloczanska, E. S. et al. Global imprint of climate change on marine life. Nat. Clim. Change 3, 919–925 (2013).ADS 

    Google Scholar 
    Bellwood, D. R., Hughes, T. P., Folke, C. & Nyström, M. Confronting the coral reef crisis. Nature 429, 827–833 (2004).ADS 
    CAS 

    Google Scholar 
    Moreno-Mateos, D. et al. Anthropogenic ecosystem disturbance and the recovery debt. Nat. Commun. 8, 14163 (2017).ADS 
    CAS 

    Google Scholar 
    Newman, E. A. Disturbance ecology in the Anthropocene. Front. Ecol. Evol. 7, 147 (2019).
    Google Scholar 
    Mittelbach, G. G. et al. What is the observed relationship between species richness and productivity?. Ecology 82, 2381–2396 (2001).
    Google Scholar 
    van Nes, E. H. & Scheffer, M. Implications of spatial heterogeneity for catastrophic regime shifts in ecosystems. Ecology 86, 1797–1807 (2005).
    Google Scholar 
    Tylianakis, J. M. et al. Resource heterogeneity moderates the biodiversity-function relationship in real world ecosystems. Plos Biol. 6, e122 (2008).
    Google Scholar 
    Loreau, M. et al. In Metacommunities: Spatial Dynamics and Ecological Communities (eds Holyoak, M. et al.) (The University of Chicago Press, 2005).
    Google Scholar 
    Loreau, M. From Populations to Ecosystems (Princeton University Press, 2010). https://doi.org/10.1515/9781400834167.vii.Book 

    Google Scholar 
    Moreira, E. F., Boscolo, D. & Viana, B. F. Spatial heterogeneity regulates plant-pollinator networks across multiple landscape scales. PLoS ONE 10, e0123628 (2015).
    Google Scholar 
    Costanza, J. K., Moody, A. & Peet, R. K. Multi-scale environmental heterogeneity as a predictor of plant species richness. Landsc. Ecol. 26, 851–864 (2011).
    Google Scholar 
    Hughes, T. P. et al. Global warming transforms coral reef assemblages. Nature 556, 492–496 (2018).ADS 
    CAS 

    Google Scholar 
    Nyström, M., Graham, N. A. J., Lokrantz, J. & Norström, A. V. Capturing the cornerstones of coral reef resilience: Linking theory to practice. Coral Reefs 27, 795–809 (2008).ADS 

    Google Scholar 
    Virah-Sawmy, M., Gillson, L. & Willis, K. J. How does spatial heterogeneity influence resilience to climatic changes? Ecological dynamics in southeast Madagascar. Ecol. Monogr. 79, 557–574 (2009).
    Google Scholar 
    Wilson, D. S. Complex interactions in metacommunities, with implications for biodiversity and higher levels of selection. Ecology 73, 1984–2000 (1992).
    Google Scholar 
    Leibold, M. A. et al. The metacommunity concept: A framework for multi-scale community ecology. Ecol. Lett. 7, 601–613 (2004).
    Google Scholar 
    Briggs, C. J. & Hoopes, M. F. Stabilizing effects in spatial parasitoid–host and predator–prey models: A review. Theor. Popul. Biol. 65, 299–315 (2004).MATH 

    Google Scholar 
    Wang, S., Haegeman, B. & Loreau, M. Dispersal and metapopulation stability. PeerJ 3, e1295 (2015).
    Google Scholar 
    Tilman, D. The ecological consequences of changes in biodiversity: A search for general principles. Ecology 80, 1455–1474 (1999).
    Google Scholar 
    Loreau, M., Mouquet, N. & Gonzalez, A. Biodiversity as spatial insurance in heterogeneous landscapes. Proc. Natl. Acad. Sci. 100, 12765–12770 (2003).ADS 
    CAS 

    Google Scholar 
    Yachi, S. & Loreau, M. Biodiversity and ecosystem productivity in a fluctuating environment: The insurance hypothesis. Proc. Natl. Acad. Sci. 96, 1463–1468 (1999).ADS 
    CAS 

    Google Scholar 
    Bouvier, T. et al. Contrasted effects of diversity and immigration on ecological insurance in marine bacterioplankton communities. PLoS ONE 7, e37620 (2012).ADS 
    CAS 

    Google Scholar 
    Hammond, M., Loreau, M., Mazancourt, C. & Kolasa, J. Disentangling local, metapopulation, and cross-community sources of stabilization and asynchrony in metacommunities. Ecosphere 11, e03078 (2020).
    Google Scholar 
    Lamy, T., Legendre, P., Chancerelle, Y., Siu, G. & Claudet, J. Understanding the spatio-temporal response of coral reef fish communities to natural disturbances: Insights from beta-diversity decomposition. PLoS ONE 10, e0138696 (2015).
    Google Scholar 
    Lamy, T. et al. Species insurance trumps spatial insurance in stabilizing biomass of a marine macroalgal metacommunity. Ecology 100, e02719 (2019).
    Google Scholar 
    Stier, A. C., Shelton, A. O., Samhouri, J. F., Feist, B. E. & Levin, P. S. Fishing, environment, and the erosion of a population portfolio. Ecosphere https://doi.org/10.1002/ecs2.3283 (2020).Article 

    Google Scholar 
    Burgess, S. C. et al. Beyond connectivity: How empirical methods can quantify population persistence to improve marine protected-area design. Ecol. Appl. 24, 257–270 (2014).
    Google Scholar 
    Saenz-Agudelo, P., Jones, G. P., Thorrold, S. R. & Planes, S. Connectivity dominates larval replenishment in a coastal reef fish metapopulation. Proc. R. Soc. B Biol. Sci. 278, 2954–2961 (2011).
    Google Scholar 
    Wood, S., Paris, C. B., Ridgwell, A. & Hendy, E. J. Modelling dispersal and connectivity of broadcast spawning corals at the global scale. Glob. Ecol. Biogeogr. 23, 1–11 (2014).
    Google Scholar 
    Loreau, M. et al. Biodiversity as insurance: From concept to measurement and application. Biol. Rev. https://doi.org/10.1111/brv.12756 (2021).Article 

    Google Scholar 
    Thibaut, L. M. & Connolly, S. R. Understanding diversity–stability relationships: Towards a unified model of portfolio effects. Ecol. Lett. 16, 140–150 (2013).
    Google Scholar 
    Wilcox, K. R. et al. Asynchrony among local communities stabilises ecosystem function of metacommunities. Ecol. Lett. 20, 1534–1545 (2017).
    Google Scholar 
    Loreau, M. & de Mazancourt, C. Species synchrony and its drivers: Neutral and nonneutral community dynamics in fluctuating environments. Am. Nat. 172, E48–E66 (2008).
    Google Scholar 
    Loreau, M. & Mazancourt, C. Biodiversity and ecosystem stability: A synthesis of underlying mechanisms. Ecol. Lett. 16, 106–115 (2013).
    Google Scholar 
    Gross, K. et al. Species richness and the temporal stability of biomass production: A new analysis of recent biodiversity experiments. Am. Nat. 183, 1–12 (2014).
    Google Scholar 
    Sullaway, G. H., Shelton, A. O. & Samhouri, J. F. Synchrony erodes spatial portfolios of an anadromous fish and alters availability for resource users. J. Anim. Ecol. https://doi.org/10.1111/1365-2656.13575 (2021).Article 

    Google Scholar 
    Adjeroud, M., Augustin, D., Galzin, R. & Salvat, B. Natural disturbances and interannual variability of coral reef communities on the outer slope of Tiahura (Moorea, French Polynesia): 1991 to 1997. Mar. Ecol. Prog. Ser. 237, 121–131 (2002).ADS 

    Google Scholar 
    Adjeroud, M. et al. Recurrent disturbances, recovery trajectories, and resilience of coral assemblages on a South Central Pacific reef. Coral Reefs 28, 775–780 (2009).ADS 

    Google Scholar 
    Pratchett, M. S., Trapon, M., Berumen, M. L. & Chong-Seng, K. Recent Disturbances Augment Community Shifts in Coral Assemblages in Moorea, French Polynesia (SpringerLink, 2011). https://doi.org/10.1007/s00338-010-0678-2.Book 

    Google Scholar 
    Kayal, M. et al. Predator crown-of-thorns starfish (Acanthaster planci) outbreak, mass mortality of corals, and cascading effects on reef fish and benthic communities. PLoS ONE 7, e47363 (2012).ADS 
    CAS 

    Google Scholar 
    McWilliam, M., Pratchett, M. S., Hoogenboom, M. O. & Hughes, T. P. Deficits in functional trait diversity following recovery on coral reefs. Proc. R. Soc. B 287, 20192628 (2020).
    Google Scholar 
    Hoegh-Guldberg, O. et al. Coral reefs under rapid climate change and ocean acidification. Science 318, 1737–1742 (2007).ADS 
    CAS 

    Google Scholar 
    Penin, L., Adjeroud, M., Schrimm, M. & Lenihan, H. S. High spatial variability in coral bleaching around Moorea (French Polynesia): Patterns across locations and water depths. C. R. Biol. 330, 171–181 (2007).
    Google Scholar 
    Adam, T. C. et al. Herbivory, connectivity, and ecosystem resilience: Response of a coral reef to a large-scale perturbation. PLoS ONE 6, e23717 (2011).ADS 
    CAS 

    Google Scholar 
    Edmunds, P. et al. Why more comparative approaches are required in time-series analyses of coral reef ecosystems. Mar. Ecol. Prog. Ser. 608, 297–306 (2019).ADS 

    Google Scholar 
    Pérez-Rosales, G. et al. Documenting decadal disturbance dynamics reveals archipelago-specific recovery and compositional change on Polynesian reefs. Mar. Pollut. Bull. 170, 112659 (2021).
    Google Scholar 
    Bruno, J. F. & Selig, E. R. Regional decline of coral cover in the Indo-Pacific: Timing, extent, and subregional comparisons. PLoS ONE 2, e711 (2007).ADS 

    Google Scholar 
    Jackson, J. B. C. et al. Status and trends of Caribbean coral reefs. Global Coral Reef Monitoring Network, IUCN, Gland, Switzerland (2014)Edmunds, P. J. Implications of high rates of sexual recruitment in driving rapid reef recovery in Mo’orea, French Polynesia. Sci. Rep. 8, 16615 (2018).ADS 

    Google Scholar 
    Burgess, S. C., Johnston, E. C., Wyatt, A. S. J., Leichter, J. J. & Edmunds, P. J. Response diversity in corals: Hidden differences in bleaching mortality among cryptic Pocillopora species. Ecology https://doi.org/10.1002/ecy.3324 (2021).Article 

    Google Scholar 
    Holbrook, S. J. et al. Recruitment drives spatial variation in recovery rates of resilient coral reefs. Sci. Rep. 8, 7338 (2018).ADS 

    Google Scholar 
    Guest, J. R. et al. A framework for identifying and characterising coral reef “oases” against a backdrop of degradation. J. Appl. Ecol. 55, 2865–2875 (2018).
    Google Scholar 
    Hench, J. L., Leichter, J. J. & Monismith, S. G. Episodic circulation and exchange in a wave-driven coral reef and lagoon system. Limnol. Oceanogr. 53, 2681–2694 (2008).ADS 

    Google Scholar 
    Barry, J. P. & Dayton, P. K. Ecological heterogeneity. Ecol. Stud. https://doi.org/10.1007/978-1-4612-3062-5_14 (1991).Article 

    Google Scholar 
    Edmunds, P. & Bruno, J. The importance of sampling scale in ecology: Kilometer-wide variation in coral reef communities. Mar. Ecol. Prog. Ser. 143, 165–171 (1996).ADS 

    Google Scholar 
    Lough, J. M., Anderson, K. D. & Hughes, T. P. Increasing thermal stress for tropical coral reefs: 1871–2017. Sci. Rep. 8, 6079 (2018).ADS 
    CAS 

    Google Scholar 
    van Oppen, M. J. H. & Lough, J. M. Coral bleaching, patterns, processes, causes and consequences. Ecol. Stud. https://doi.org/10.1007/978-3-319-75393-5_14 (2018).Article 

    Google Scholar 
    Monismith, S. G. Hydrodynamics of coral reefs. Annu. Rev. Fluid Mech. 39, 37–55 (2007).ADS 
    MATH 

    Google Scholar 
    Edmunds P. Of Moorea Coral Reef LTER. MCR LTER: Coral Reef: Long-term Population and Community Dynamics: Corals, ongoing since 2005. knb-lter-mcr.4.33 https://doi.org/10.6073/pasta/1f05f1f52a2759dc096da9c24e88b1e8 (2020).Cowles, J. et al. Resilience: insights from the U.S. Long-term ecological research network. Ecosphere 12, e03434 (2021).
    Google Scholar 
    Beijbom, O. et al. Towards automated annotation of benthic survey images: Variability of human experts and operational modes of automation. PLoS ONE 10, e0130312 (2015).
    Google Scholar 
    Veron, J. E. N. Corals of the world, v. 1–3. Australian Institute of Marine Science (2000)Washburn, L of Moorea Coral Reef LTER. MCR LTER: Coral Reef: Ocean Currents and Biogeochemistry: salinity, temperature and current at CTD and ADCP mooring FOR01 from 2004 ongoing. knb-lter-mcr.30.36doi:10.6073/pasta/124d19950c5234bf1937661989dcced7 (2021).Safaie, A. et al. High frequency temperature variability reduces the risk of coral bleaching. Nat. Commun. 9, 1671 (2018).ADS 

    Google Scholar 
    Dean, R. G. & Dalrymple, R. A. Water Wave Mechanics for Engineers and Scientists. Advanced Series on Ocean Engineering Vol. 2 (World Scientific, 1991).
    Google Scholar 
    Carroll, A., Harrison, P. & Adjeroud, M. Sexual reproduction of Acropora reef corals at Moorea, French Polynesia. Coral Reefs 25, 93–97 (2006).ADS 

    Google Scholar 
    Han, X., Adam, T. C., Schmitt, R. J., Brooks, A. J. & Holbrook, S. J. Response of herbivore functional groups to sequential perturbations in Moorea, French Polynesia. Coral Reefs 35, 999–1009 (2016).ADS 

    Google Scholar 
    Clarke, K. R. Non-parametric multivariate analyses of changes in community structure. Austral Ecol. 18, 117–143 (1993).
    Google Scholar 
    Clarke, K. R., Somerfield, P. J. & Chapman, M. G. On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray–Curtis coefficient for denuded assemblages. J. Exp. Mar. Biol. Ecol. 330, 55–80 (2006).
    Google Scholar 
    RStudio Team. RStudio: Integrated development for R. RStudio, PBC, Boston, MA URL http://www.rstudio.com/ (2021).Oksanen J. et al. vegan: Community ecology package. R package version 2.5–7. https://CRAN.R-project.org/package=vegan (2020).Wickham, et al. Welcome to the Tidyverse. J. Open Source Softw. 4(43), 1686. https://doi.org/10.21105/joss.01686 (2019).Article 
    ADS 

    Google Scholar 
    Corlett, R. T. The Anthropocene concept in ecology and conservation. Trends Ecol. Evol. 30, 36–41 (2015).
    Google Scholar 
    Williams, G. J. et al. Coral reef ecology in the Anthropocene. Funct. Ecol. 33, 1014–1022 (2019).
    Google Scholar 
    Walther, G.-R. et al. Ecological responses to recent climate change. Nature 416, 389–395 (2002).ADS 
    CAS 

    Google Scholar 
    Walther, G.-R. Community and ecosystem responses to recent climate change. Philos. Trans. R. Soc. B Biol. Sci. 365, 2019–2024 (2010).
    Google Scholar 
    Cinner, J. E. et al. Bright spots among the world’s coral reefs. Nature 535, 416–419 (2016).ADS 
    CAS 

    Google Scholar 
    Grman, E., Lau, J. A., Schoolmaster, D. R. & Gross, K. L. Mechanisms contributing to stability in ecosystem function depend on the environmental context. Ecol. Lett. 13, 1400–1410 (2010).
    Google Scholar 
    Schindler, D. E. et al. Population diversity and the portfolio effect in an exploited species. Nature 465, 609–612 (2010).ADS 
    CAS 

    Google Scholar 
    Doak, D. F. et al. The statistical inevitability of stability-diversity relationships in community ecology. Am. Nat. 151, 264–276 (1998).CAS 

    Google Scholar 
    Isbell, F. I., Polley, H. W. & Wilsey, B. J. Biodiversity, productivity and the temporal stability of productivity: Patterns and processes. Ecol. Lett. 12, 443–451 (2009).
    Google Scholar 
    Connell, J. H. Diversity in tropical rain forests and coral reefs author. Science 199, 1302–1310 (1978).ADS 
    CAS 

    Google Scholar 
    Plaisance, L., Caley, M. J., Brainard, R. E. & Knowlton, N. The diversity of coral reefs: What are we missing?. PLoS ONE 6, e25026 (2011).ADS 
    CAS 

    Google Scholar 
    Williams, G. J. et al. Biophysical drivers of coral trophic depth zonation. Mar. Biol. 165, 60 (2018).
    Google Scholar 
    Moritz, C. et al. Long-term monitoring of benthic communities reveals spatial determinants of disturbance and recovery dynamics on coral reefs. Mar. Ecol. Prog. Ser. 672, 141–152 (2021).ADS 

    Google Scholar 
    Dietzel, A. et al. The spatial footprint and patchiness of large scale disturbances on coral reefs. Global Change Biol. 27, 4825–4838 (2021).CAS 

    Google Scholar 
    Leichter, J. et al. Biological and physical interactions on a tropical island coral reef: Transport and retention processes on Moorea, French Polynesia. Oceanography 26, 52–63 (2011).
    Google Scholar 
    Porter, J. W. et al. Population trends among Jamaican reef corals. Nature 294, 249–250 (1981).ADS 

    Google Scholar 
    Graham, N. A. J., Jennings, S., MacNeil, M. A., Mouillot, D. & Wilson, S. K. Predicting climate-driven regime shifts versus rebound potential in coral reefs. Nature 518, 94–97 (2015).ADS 
    CAS 

    Google Scholar 
    Whittaker, R. H. & Levin, S. A. The role of mosaic phenomena in natural communities. Theor. Popul. Biol. 12, 117–139 (1977).CAS 

    Google Scholar 
    Karlson, R. H. & Hurd, L. E. Disturbance, coral reef communities, and changing ecological paradigms. Coral Reefs 12, 117–125 (1993).ADS 

    Google Scholar 
    Stoddart, D. R. Effects of Hurricane Hattie on the British Honduras reefs and cays, October 30–31, 1961. Atoll Res. Bull. 95, 1–142 (1963).
    Google Scholar 
    Witman, J. D. Physical disturbance and community structure of exposed and protected reefs: A case study from St. John U.S. Virgin Islands. Integr. Comp. Biol. 32, 641–654 (1992).
    Google Scholar 
    Thorson, J. T., Scheuerell, M. D., Olden, J. D. & Schindler, D. E. Spatial heterogeneity contributes more to portfolio effects than species variability in bottom-associated marine fishes. Proc. R. Soc. B 285, 20180915 (2018).
    Google Scholar 
    Mellin, C., MacNeil, M. A., Cheal, A. J., Emslie, M. J. & Caley, M. J. Marine protected areas increase resilience among coral reef communities. Ecol. Lett. 19, 629–637 (2016).
    Google Scholar 
    Beyer, H. L. et al. Risk-sensitive planning for conserving coral reefs under rapid climate change. Conserv. Lett. 11, e12587 (2018).
    Google Scholar 
    Harrison, H. B., Bode, M., Williamson, D. H., Berumen, M. L. & Jones, G. P. A connectivity portfolio effect stabilizes marine reserve performance. Proc. Natl. Acad. Sci. 117, 25595–25600 (2020).ADS 
    CAS 

    Google Scholar 
    Walter, J. A. et al. The spatial synchrony of species richness and its relationship to ecosystem stability. Ecology https://doi.org/10.1002/ecy.3486 (2021).Article 

    Google Scholar 
    Wang, S., Lamy, T., Hallett, L. M. & Loreau, M. Stability and synchrony across ecological hierarchies in heterogeneous metacommunities: Linking theory to data. Ecography 42, 1200–1211 (2019).
    Google Scholar 
    Catano, C. P., Fristoe, T. S., LaManna, J. A. & Myers, J. A. Local species diversity, β-diversity and climate influence the regional stability of bird biomass across North America. Proc. R. Soc. B 287, 20192520 (2020).
    Google Scholar 
    Roscher, C. et al. Identifying population- and community-level mechanisms of diversity–stability relationships in experimental grasslands. J. Ecol. 99, 1460–1469 (2011).
    Google Scholar 
    Downing, A. L., Brown, B. L. & Leibold, M. A. Multiple diversity–stability mechanisms enhance population and community stability in aquatic food webs. Ecology 95, 173–184 (2014).
    Google Scholar 
    Moran, P. The statistical analysis of the Canadian Lynx cycle. Aust. J. Zool. 1, 291–298 (1953).
    Google Scholar 
    Townsend, D. L. & Gouhier, T. C. Spatial and interspecific differences in recruitment decouple synchrony and stability in trophic metacommunities. Theor. Ecol. 12, 319–327 (2019).
    Google Scholar 
    Yeager, M. E., Gouhier, T. C. & Hughes, A. R. Predicting the stability of multitrophic communities in a variable world. Ecology 101, e02992 (2020).
    Google Scholar 
    Hughes, T. P. et al. Emergent properties in the responses of tropical corals to recurrent climate extremes. Curr. Biol. https://doi.org/10.1016/j.cub.2021.10.046 (2021).Article 

    Google Scholar 
    Jackson, J. B. C. Morphological strategies of sessile animals. In Biology and Systematics of Colonial Organisms (eds Larwood, G. & Rosen, B. R.) 499–555 (Academic, 1979).
    Google Scholar 
    Sammarco, P. W. & Andrews, J. C. Localized dispersal and recruitment in Great Barrier Reef Corals: The helix experiment. Science 239, 1422–1424 (1988).ADS 
    CAS 

    Google Scholar 
    Edmunds, P. J. Unusually high coral recruitment during the 2016 El Niño in Mo’orea, French Polynesia. PLoS ONE 12, e0185167 (2017).
    Google Scholar 
    Bull, G. Distribution and abundance of coral plankton. Coral Reefs 4, 197–200 (1986).ADS 

    Google Scholar 
    Hodgson, G. Abundance and distribution of planktonic coral larvae in Kaneohe Bay, Oahu, Hawaii. Mar. Ecol. Prog. Ser. 26, 61–71 (1985).ADS 

    Google Scholar 
    Edmunds, P. J. Vital rates of small reef corals are associated with variation in climate. Limnol. Oceanogr. 66, 901–913 (2021).ADS 

    Google Scholar  More

  • in

    Benthic biota of Chilean fjords and channels in 25 years of cruises of the National Oceanographic Committee

    The data were recorded under the DarwinCore standard55,56 in a matrix named “Benthic biota of CIMAR-Fiordos and Southern Ice Field Cruises”58. The occurrence dataset contains direct basic information (description, scope [temporal, geographic and taxonomic], methodology, bibliography, contacts, data description, GBIF registration and citation), project details, metrics (taxonomy and occurrences classification), activity (citations and download events) and download options. The following data fields were occupied:Column 1: “occurrenceID” (single indicator of the biological record indicating the cruise and correlative record).Column 2: “basisOfRecord” (“PreservedSpecimen” for occurrence records with catalogue number of scientific collection, “MaterialCitation” for any literature record).Column 3: “institutionCode” (The acronym in use by the institution having custody of the sample or information referred to in the record).Column 4: “collectionCode” (The name of the cruise).Column 5: “catalogNumber” (The repository number in museums or correlative number).Column 6: “type” (All records entered as “text”).Column 7: “language” (Spanish, English or both).Column 8: “institutionID” (The identifier for the institution having custody of the sample or information referred to in the record).Column 9: “collectionID” (The identifier for the collection or dataset from which the record was derived).Column 10: “datasetID” (The code “CONA-benthic-biota-database” for entire database).Column 11: “recordedBy” (Author/s who recorded the original occurrence [publication source]).Column 12: “individualCount” (Number of individuals recorded).Column 13: “associatedReferences” (Publication source [report and/or paper/s] for each record).Column 14: “samplingProtocol” (The sampling gear for each record).Column 15: “eventDate” (The date-time or interval during which the record occurred).Column 16: “eventRemarks” (Comments or notes about the event).Column 17: “continent” (Location).Column 18: “country” (Location).Column 19: “countryCode” (The standard code for the country in which the location occurs).Column 20: “stateProvince” (Location, refers to the Administrative Region of Chile).Column 21: “county” (Location, refers to the Administrative Province of Chile).Column 22: “municipality” (Location, refers to the Administrative Commune of Chile).Column 23: “locality” (The specific name of the place).Column 24: “verbatimLocality” (The original textual description of the place).Column 25: “verbatimDepth” (The original description of the depth).Column 26: “minimumDepthInMeters” (The shallowest depth of a range of depths).Column 27: “maximumDepthInMeters” (The deepest depth of a range of depths).Column 28: “locationRemarks” (The name of the sample station of the cruise).Column 29: “verbatimLatitude” (The verbatim original latitude of the location).Column 30: “verbatimLongitude” (The verbatim original longitude of the location).Column 31: “verbatimCoordinateSystem” (The coordinate format for the “verbatimLatitude” and “verbatimLongitude” or the “verbatimCoordinates” of the location).Column 32: “verbatimSRS” (The spatial reference system [SRS] upon which coordinates given in “verbatimLatitude” and “verbatimLongitude” are based)Column 33: “decimalLatitude” (The geographic latitude in decimal degrees).Column 34: “decimalLongitude” (The geographic longitude in decimal degrees).Column 35: “geodeticDatum” (The spatial reference system [SRS] upon which the geographic coordinates given in “decimalLatitude” and “decimalLongitude” was based).Column 36: “coordinateUncertaintyInMeters” (The horizontal distance from the given “decimalLatitude” and “decimalLongitude” describing the smallest circle containing the whole of the location).Column 37: “georeferenceRemarks” (Notes about the spatial description determination).Column 38: “identifiedBy” (Responsible for recording the original occurrence [publication source]).Column 39: “dateIdentified” (The date-time or interval during which the identification occurred.)Column 40: “identificationQualifier” (A taxonomic determination [e.g., “sp.”, “cf.”]).Column 41: “scientificNameID” (An identifier for the nomenclatural details of a scientific name).Column 42: “scientificName” (The name of species or taxon of the occurrence record).Column 43: “kingdom” (The scientific name of the kingdom in which the taxon is classified).Column 44: “phylum” (The scientific name of the phylum or division in which the taxon is classified).Column 45: “class” (The scientific name of the class in which the taxon is classified).Column 46: “order” (The scientific name of the order in which the taxon is classified).Column 47: “family” (The scientific name of the family in which the taxon is classified).Column 48: “genus” (The scientific name of the genus in which the taxon is classified).Column 49: “subgenus” (The scientific name of the subgenus in which the taxon is classified).Column 50: “specificEpithet” (The name of the first or species epithet of the “scientificName”).Column 51: “infraspecificEpithet” (The name of the lowest or terminal infraspecific epithet of the “scientificName”).Column 52: “taxonRank” (The taxonomic rank of the most specific name in the “scientificName”).Column 53: “scientificNameAuthorship” (The authorship information for the “scientificName” formatted according to the conventions of the applicable nomenclatural Code).Column 54: “verbatimIdentification” (A string representing the taxonomic identification as it appeared in the original record).The information sources (see Fig. 2b) provided a total of 107 publications (22 cruise reports and 85 scientific papers; see Fig. 2c). Nineteen of the 22 cruise reports reviewed provided species occurrence records8,28,29,30,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46, one provided qualitative or descriptive data, with no recorded occurrences31, and two did not provide information on benthic biota (CIMAR-9 and −23 cruises). Of all the scientific papers reviewed, 74 provided records of species occurrences (Table 2), while 11 did not provide any record, as they were data without occurrences of geographically referenced species or with descriptive or qualitative information: Foraminifera59,60,61,62, Annelida63,64,65,66, Fishes67, Mollusca68 and Echinodermata69. The phyla with the highest number of publications were the following: Annelida (present in 18 reports and 21 papers), Mollusca (in 14 and 20), Arthropoda (in 10 and 18), Echinodermata (in 10 and 9), Chordata (in 10 and 9) and Foraminifera (in 4 and 10).Table 2 Publications with >100 occurrences, indicating the main recorded taxa.Full size tableThe information registry includes data on occurrences and number of individuals for 8,854 records (files in the database), representing 1,225 species (Fig. 3). The main taxa in terms of occurrence and number of species were Annelida (mainly Polychaeta), Foraminifera, Mollusca and Arthopoda (mainly Crustacea), together accumulating ~70% of total occurrences and ~73% of the total species (Fig. 3). The large number of recorded occurrences of Myzozoa (10%) should be highlighted, which, however, only represent about 32 species. Echinodermata represented ~8% of occurrences and 7% of species.Fig. 3Occurrences and total species by taxon, considering large taxonomic groups of the benthic biota recorded in the CIMAR 1 to 25 and CDHS-1995 cruises. The absolute values of occurrences and species are represented in parentheses.Full size imageThe cruises with the highest number of occurrences were CIMAR-2 (with 1,424), followed by CIMAR-8 (1,040) and CIMAR-16 (813) (Fig. 4). Three dominant taxonomic groups were recorded in most cruises, except for cruises CIMAR-1, CIMAR-4, CIMAR-17, CIMAR-18 and CIMAR-24 (Fig. 4). The cruises with the highest number of species recorded were CIMAR-2 (with 335), CIMAR-3 (328) and CIMAR-8 (323) (Fig. 5). Three or fewer dominant taxonomic groups were recorded only in the CIMAR-1, CIMAR-4, CIMAR-17, CIMAR-18 and CIMAR-24 cruises (Fig. 5).Fig. 4Total occurrences and percentages per dominant taxon recorded in each of the CIMAR 1 to 25 and CDHS-1995 cruises. The absolute values of occurrences per dominant taxon are represented in parentheses.Full size imageFig. 5Total species and percentages per dominant taxon recorded in each of the CIMAR 1 to 25 and CDHS-1995 cruises. The absolute values of species per dominant taxon are represented in parentheses.Full size imageThe latitudinal bands 42°S and 45°S are those with the highest number of occurrences (Fig. 6), while the 56°S and 46°S bands had the fewest. The highest number of species was recorded in the 52°S and 50°S latitudinal bands, while, as with the occurrences, the lowest values corresponded to the 56°S and 46°S latitudinal bands (Fig. 6).Fig. 6Occurrences and number of species recorded by latitudinal band from the CIMAR 1 to 25 and CDHS-1995 cruises. SEP: South-eastern Pacific.Full size image More

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    Genetic population structures of common scavenging species near hydrothermal vents in the Okinawa Trough

    Van Dover, C. L. et al. Environmental management of deep-sea chemosynthetic ecosystems: justification of and considerations for a spatially based approach. ISA Technical Study: No.9. (International Seabed Authority, 2011).Ikehata, K., Suzuki, R., Shimada, K., Ishibashi, J., & Urabe, T. Mineralogical and Geochemical Characteristics of Hydrothermal Minerals Collected from Hydrothermal Vent Fields in the Southern Mariana Spreading Center. In Subseafloor biosphere linked to hydrothermal systems: TAIGA Concept. 275–288 (Springer Tokyo, 2015).Rona, P. A. & Scott, S. D. A special issue on sea-floor hydrothermal mineralization; new perspectives; preface. Econ. Geol. 88, 1935–1976 (1993).
    Google Scholar 
    Glasby, G. P., Iizasa, K., Yuasa, M. & Usui, A. Submarine hydrothermal mineralization on the Izu-Bonin arc, south of Japan: an overview. Mar. Georesources Geotech. 18, 141–176 (2000).
    Google Scholar 
    Van Dover, C. L. Inactive sulfide ecosystems in the deep sea: a review. Front. Mar. Sci. 6, 461. https://doi.org/10.3389/fmars.2019.00461 (2019).Article 

    Google Scholar 
    Boschen, R. E., Rowde, A. A., Clark, M. R. & Gardner, J. P. Mining of deep-sea seafloor massive sulfides: a review of the deposits, their benthic communities, impacts from mining, regulatory frameworks and management strategies. Ocean Coast. Manag. 84, 54–67 (2013).
    Google Scholar 
    Washburn, T. W. et al. Ecological risk assessment for deep-sea mining. Ocean Coast. Manag. 176, 24–39 (2019).
    Google Scholar 
    Matsui, T., Sugishima, H., Okamoto, N., Igarashi, Y. Evaluation of turbidity and resedimentation through seafloor disturbance experiments for assessment of environmental impacts associated with exploitation of seafloor massive sulfides mining. Proceedings of the Twenty-eighth. International Ocean and Polar Engineering Conference. 144–151 (2018).International Seabed Authority. Recommendations for the guidance of contractors for the assessment of the possible environmental impacts arising from exploration for marine minerals in the Area. https://www.isa.org.jm/documents/isba19ltc8 (2013).Suzuki, K., Yoshida, K., Watanabe, H. & Yamamoto, H. Mapping the resilience of chemosynthetic communities in hydrothermal vent fields. Sci. Rep. 8, 9364. https://doi.org/10.1038/s41598-018-27596-7 (2018).Article 
    ADS 
    CAS 

    Google Scholar 
    Yahagi, T., Watanabe, H., Ishibashi, J. I. & Kojima, S. Genetic population structure of four hydrothermal vent shrimp species (Alvinocarididae) in the Okinawa Trough, Northwest Pacific. Mar. Ecol. Prog. Ser. 529, 159–169 (2015).ADS 

    Google Scholar 
    Mullineaux, L. S. Deep-sea hydrothermal vent communities. In Marine community ecology and conservation (eds Bertness, M. D. et al.) 383–400 (Sinauer, 2013).
    Google Scholar 
    Van Dover, C. L., German, C. R., Speer, K. G., Parson, L. M. & Vrijenhoek, R. C. Evolution and biogeography of deep-sea vent and seep invertebrates. Science 295, 1253–1257 (2002).ADS 

    Google Scholar 
    Yahagi, T., Kayama-Watanabe, H., Kojima, S. & Kano, Y. Do larvae from deep-sea hydrothermal vents disperse in surface waters?. Ecology 98, 1524–1534 (2017).
    Google Scholar 
    Hebert, P. D. & Gregory, T. R. The promise of DNA barcoding for taxonomy. Syst. Biol. 54, 852–859 (2005).
    Google Scholar 
    Iguchi, A. et al. Comparative analysis on the genetic population structures of the deep-sea whelks Buccinum tsubai and Neptunea constricta in the Sea of Japan. Mar. Biol. 151, 31–39 (2007).
    Google Scholar 
    Goode, G. B. & Bean, T. H. A catalogue of the fishes of Essex County, Massachusetts, including the fauna of Massachusetts Bay and the contiguous deep waters. Bull. Essex Inst. 11, 1–38 (1879).
    Google Scholar 
    Johnson, J. Y. Descriptions of some new genera and species of fishes obtained at Madeira. Proc. Zool. Soc. Lond. 1862, 167–180 (1862).
    Google Scholar 
    Bate, C. S. Report on the Crustacea Macrura collected by the Challenger during the years 1873–76. Report on the scientific results of the Voyage of H.M.S. Challenger during the years 1873–76. Zoology 24, 1–942 (1888).
    Google Scholar 
    Folmer, O., Black, M., Hoeh, W. R., Lutz, R. & Vrijenhoek, R. C. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol Biotech. 3, 294–299 (1994).CAS 

    Google Scholar 
    Pilgrim, E. M., Blum, M. J., Reusser, D. A., Lee, H. & Darling, J. A. Geographic range and structure of cryptic genetic diversity among Pacific North American populations of the non-native amphipod Grandidierella japonica. Biol. Invasions 15, 2415–2428 (2013).
    Google Scholar 
    Suyama, Y. & Matsuki, Y. MIG-seq: an effective PCR-based method for genome-wide single-nucleotide polymorphism genotyping using the next-generation sequencing platform. Sci. Rep. 5, 16963. https://doi.org/10.1038/srep16963 (2015).Article 
    ADS 
    CAS 

    Google Scholar 
    R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/ (2020).Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).CAS 

    Google Scholar 
    Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).CAS 

    Google Scholar 
    Shen, W., Le, S., Li, Y. & Hu, F. SeqKit: a cross-platform and ultrafast toolkit for FASTA/Q file manipulation. PLoS ONE 11, e0163962. https://doi.org/10.1371/journal.pone.0163962 (2016).Article 
    CAS 

    Google Scholar 
    Paradis, E. pegas: an R package for population genetics with an integrated–modular approach. Bioinformatics 26, 419–420 (2010).CAS 

    Google Scholar 
    Kumar, S., Stecher, G. & Tamura, K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874 (2016).CAS 

    Google Scholar 
    Darriba, D. et al. ModelTest-NG: a new and scalable tool for the selection of DNA and protein evolutionary models. Mol. Biol. Evol. 37, 291–294 (2020).CAS 

    Google Scholar 
    Kozlov, A. M., Darriba, D., Flouri, T., Morel, B. & Stamatakis, A. RaxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35, 4453–4455 (2019).CAS 

    Google Scholar 
    Ronquist, F. R. & Huelsenbeck, J. P. MRBAYES 3: Bayesian inference of phylogeny. Bioinformatics 19, 1572–1574 (2003).CAS 

    Google Scholar 
    Puillandre, N., Brouillet, S. & Achaz, G. ASAP: assemble species by automatic partitioning. Mol. Ecol. Resour. 21, 609–620 (2021).
    Google Scholar 
    Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17, http://journal.embnet.org/index.php/embnetjournal/article/view/200/479 (2011).Rochette, N. C., Rivera-Colón, A. G. & Catchen, J. M. Stacks 2: Analytical methods for paired-end sequencing improve RADseq-based population genomics. Mol. Ecol. 28, 4737–4754 (2019).CAS 

    Google Scholar 
    Purcell, S. et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575 (2007).CAS 

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

    Google Scholar 
    Goudet, J. Hierfstat, a package for R to compute and test hierarchical F-statistics. Mol. Ecol. Notes 5, 184–186 (2013).
    Google Scholar 
    Oksanen, J. et al. vegan: Community Ecology Package. R package version 2.5–6. https://CRAN.R-project.org/package=vegan (2019).Dana, J. D. Synopsis of the genera of Gammaracea. Am. J. Sci. Arts 8, 135–140 (1849).
    Google Scholar 
    Hansen, H. J. Malacostraca marina Groenlandiæ occidentalis Oversigt over det vestlige Grønlands Fauna af malakostrake Havkrebsdyr. Vidensk. Meddel. Natuirist. Foren Kjobenhavn, Aaret 9, 5–226 (1888).
    Google Scholar 
    Van Dover, C. L. The ecology of deep-sea hydrothermal vents (Princeton University Press, 2000).
    Google Scholar 
    Tunnicliffe, V. The biology of hydrothermal vents: ecology and evolution. Oceanogr. Mar. Biol. Annu. Rev. 29, 319–407 (1991).
    Google Scholar 
    Priede, I. G., Bagley, P. M., Smith, A., Creasey, S. & Merrett, N. R. Scavenging deep demersal fishes of the Porcupine Seabight, north-east Atlantic: observations by baited camera, trap and trawl. J. Mar. Biol. Assoc. U. K. 74, 481–498 (1994).
    Google Scholar 
    Causse, R., Biscoito, M. & Briand, P. First record of the deep-sea eel Ilyophis saldanhai (Synaphobranchidae, Anguilliformes) from the Pacific Ocean. Cybium 29, 413–416 (2005).
    Google Scholar 
    King, N. J., Bagley, P. M. & Priede, I. G. Depth zonation and latitudinal distribution of deep-sea scavenging demersal fishes of the Mid-Atlantic Ridge, 42 to 53°N. Mar. Ecol. Prog. Ser. 319, 263–274 (2006).ADS 

    Google Scholar 
    Leitner, A. B., Durden, J. M., Smith, C. R., Klingberg, E. D. & Drazen, J. C. Synaphobranchid eel swarms on abyssal seamounts: largest aggregation of fishes ever observed at abyssal depths. Deep Sea Res. Oceanogr. Res. Part I Pap. 167, 103423. https://doi.org/10.1016/j.dsr.2020.103423 (2021).Article 

    Google Scholar 
    Fishelson, L. Comparative internal morphology of deep-sea eels, with particular emphasis on gonads and gut structure. J. Fish. Biol. 44, 75–101 (1994).
    Google Scholar 
    Bailey, D. M. et al. High swimming and metabolic activity in the deep-sea eel Synaphobranchus kaupii revealed by integrated in situ and in vitro measurements. Physiol. Biochem. Zool. 78, 335–346 (2005).
    Google Scholar 
    Trenkel, V. M. & Lorance, P. Estimating Synaphobranchus kaupii densities: contribution of fish behaviour to differences between bait experiments and visual strip transects. Deep Sea Res. Oceanogr. Res. Part I Pap. 58, 63–71 (2011).ADS 

    Google Scholar 
    Raupach, M. J. et al. Genetic homogeneity and circum-Antarctic distribution of two benthic shrimp species of the Southern Ocean, Chorismus antarcticus and Nematocarcinus lanceopes. Mar. Biol. 157, 1783–1797 (2010).CAS 

    Google Scholar 
    Dambach, J., Raupach, M. J., Leese, F., Schwarzer, J. & Engler, J. O. Ocean currents determine functional connectivity in an Antarctic deep-sea shrimp. Mar. Ecol. 37, 1336–1344 (2016).ADS 
    CAS 

    Google Scholar 
    Dambach, J., Raupach, M. J., Mayer, C., Schwarzer, J. & Leese, F. Isolation and characterization of nine polymorphic microsatellite markers for the deep-sea shrimp Nematocarcinus lanceopes (Crustacea: Decapoda: Caridea). BMC Res. Notes 6, 75. https://doi.org/10.1186/1756-0500-6-75 (2013).Article 

    Google Scholar 
    Ritchie, H., Jamieson, A. J. & Piertney, S. B. Phylogenetic relationships among hadal amphipods of the Superfamily Lysianassoidea: Implications for taxonomy and biogeography. Deep Sea Res. Part I 105, 119–131 (2015).CAS 

    Google Scholar 
    Bowen, B. W. et al. Phylogeography unplugged: comparative surveys in the genomic era. Bull. Mar. Sci. 90, 13–46 (2014).
    Google Scholar 
    Ritchie, H., Jamieson, A. J. & Piertney, S. B. Population genetic structure of two congeneric deep-sea amphipod species from geographically isolated hadal trenches in the Pacific Ocean. Deep Sea Res. Part I. 119, 50–57 (2017).
    Google Scholar 
    Iguchi, A. et al. Deep-sea amphipods around cobalt-rich ferromanganese crusts: taxonomic diversity and selection of candidate species for connectivity analysis. PLoS ONE 15, e0228483. https://doi.org/10.1371/journal.pone.0228483 (2020).Article 
    CAS 

    Google Scholar 
    Baco, A. R. et al. A synthesis of genetic connectivity in deep-sea fauna and implications for marine reserve design. Mol. Ecol. 25, 3276–3298 (2016).
    Google Scholar 
    Taylor, M. L. & Roterman, C. N. Invertebrate population genetics across Earth’s largest habitat: the deep-sea floor. Mol. Ecol. 26, 4872–4896 (2017).CAS 

    Google Scholar  More

  • in

    Multilayer networks of plasmid genetic similarity reveal potential pathways of gene transmission

    WHO. Global antimicrobial resistance and use surveillance system (GLASS) report: 2021; https://apps.who.int/iris/bitstream/handle/10665/341666/9789240027336-eng.pdfVan Boeckel TP, Glennon EE, Chen D, Gilbert M, Robinson TP, Grenfell BT, et al. Reducing antimicrobial use in food animals. Science. 2017;357:1350–2. https://doi.org/10.1126/science.aao1495Article 
    CAS 

    Google Scholar 
    ONeill J. Antimicrobials in agriculture and the environment: reducing unnecessary use and waste. Rev Antimicrob Resistance; 2015:1–28.Van Boeckel TP, Brower C, Gilbert M, Grenfell BT, Levin SA, Robinson TP, et al. Global trends in antimicrobial use in food animals. Proc Natl Acad Sci USA. 2015;112:5649–54. https://doi.org/10.1073/pnas.1503141112Article 
    CAS 

    Google Scholar 
    Managaki S, Murata A, Takada H, Tuyen BC, Chiem NH. Distribution of macrolides, sulfonamides, and trimethoprim in tropical waters: ubiquitous occurrence of veterinary antibiotics in the Mekong Delta. Environ Sci Technol. 2007;41:8004–10. https://doi.org/10.1021/es0709021Article 
    CAS 

    Google Scholar 
    Woolhouse M, Ward M, van Bunnik B, Farrar J. Antimicrobial resistance in humans, livestock and the wider environment. Philos Trans R Soc Lond B Biol Sci. 2015;370:20140083 https://doi.org/10.1098/rstb.2014.0083Article 
    CAS 

    Google Scholar 
    Noyes NR, Yang X, Linke LM, Magnuson RJ, Cook SR, Zaheer R, et al. Characterization of the resistome in manure, soil and wastewater from dairy and beef production systems. Sci Rep. 2016;6:24645. https://doi.org/10.1038/srep24645Article 
    CAS 

    Google Scholar 
    Agga GE, Cook KL, Netthisinghe AMP, Gilfillen RA, Woosley PB, Sistani KR. Persistence of antibiotic resistance genes in beef cattle backgrounding environment over two years after cessation of operation. PLoS One. 2019;14:e0212510. https://doi.org/10.1371/journal.pone.0212510Article 
    CAS 

    Google Scholar 
    Hudson JA, Frewer LJ, Jones G, Brereton PA, Whittingham MJ, Stewart G. The agri-food chain and antimicrobial resistance: a review. Trends Food Sci Technol. 2017;69:131–47. https://doi.org/10.1016/j.tifs.2017.09.007Article 
    CAS 

    Google Scholar 
    Gillings MR. Lateral gene transfer, bacterial genome evolution, and the Anthropocene. Ann NY Acad Sci. 2017;1389:20–36. https://doi.org/10.1111/nyas.13213Article 

    Google Scholar 
    Rodríguez-Beltrán J, DelaFuente J, León-Sampedro R, MacLean RC, San Millán Á. Beyond horizontal gene transfer: the role of plasmids in bacterial evolution. Nat Rev Microbiol. 2021;6:347–59. https://doi.org/10.1038/s41579-020-00497-1Article 
    CAS 

    Google Scholar 
    Zhang T, Zhang XX, Ye L. Plasmid metagenome reveals high levels of antibiotic resistance genes and mobile genetic elements in activated sludge. PLoS One. 2011;6:e26041. https://doi.org/10.1371/journal.pone.0026041Article 
    CAS 

    Google Scholar 
    Li AD, Li LG, Zhang T. Exploring antibiotic resistance genes and metal resistance genes in plasmid metagenomes from wastewater treatment plants. Front Microbiol. 2015;6:1025. https://doi.org/10.3389/fmicb.2015.01025Article 

    Google Scholar 
    Bukowski M, Piwowarczyk R, Madry A, Zagorski-Przybylo R, Hydzik M, Wladyka B. Prevalence of antibiotic and heavy metal resistance determinants and virulence-related genetic elements in plasmids of Staphylococcus aureus. Front Microbiol. 2019;10:805. https://doi.org/10.3389/fmicb.2019.00805Article 

    Google Scholar 
    Ramírez-Díaz MI, Díaz-Magaña A, Meza-Carmen V, Johnstone L, Cervantes C, Rensing C. Nucleotide sequence of Pseudomonas aeruginosa conjugative plasmid pUM505 containing virulence and heavy-metal resistance genes. Plasmid. 2011;66:7–18. https://doi.org/10.1016/j.plasmid.2011.03.002Article 
    CAS 

    Google Scholar 
    Haenni M, Poirel L, Kieffer N, Châtre P, Saras E, Métayer V, et al. Co-occurrence of extended spectrum β lactamase and MCR-1 encoding genes on plasmids. Lancet Infect Dis. 2016;16:281–2. https://doi.org/10.1016/S1473-3099(16)00007-4Article 
    CAS 

    Google Scholar 
    Peter S, Bosio M, Gross C, Bezdan D, Gutierrez J, Oberhettinger P, et al. Tracking of antibiotic resistance transfer and rapid plasmid evolution in a hospital setting by nanopore sequencing. mSphere. 2020;5. https://doi.org/10.1128/mSphere.00525-20Halary S, Leigh JW, Cheaib B, Lopez P, Bapteste E. Network analyses structure genetic diversity in independent genetic worlds. Proc Natl Acad Sci USA. 2010;107:127–32. https://doi.org/10.1073/pnas.0908978107Article 

    Google Scholar 
    Bosi E, Fani R, Fondi M. The mosaicism of plasmids revealed by atypical genes detection and analysis. BMC Genom. 2011;12:403. https://doi.org/10.1186/1471-2164-12-403Article 
    CAS 

    Google Scholar 
    Pesesky MW, Tilley R, Beck DAC. Mosaic plasmids are abundant and unevenly distributed across prokaryotic taxa. Plasmid. 2019;102:10–18. https://doi.org/10.1016/j.plasmid.2019.02.003Article 
    CAS 

    Google Scholar 
    Casjens SR, Gilcrease EB, Vujadinovic M, Mongodin EF, Luft BJ, Schutzer SE, et al. Plasmid diversity and phylogenetic consistency in the Lyme disease agent Borrelia burgdorferi. BMC Genom. 2017;18:165. https://doi.org/10.1186/s12864-017-3553-5Article 
    CAS 

    Google Scholar 
    Madec JY, Haenni M. Antimicrobial resistance plasmid reservoir in food and food-producing animals. Plasmid. 2018;99:72–81. https://doi.org/10.1016/j.plasmid.2018.09.001Article 
    CAS 

    Google Scholar 
    Ceccarelli D, Kant A, van Essen-Zandbergen A, Dierikx C, Hordijk J, Wit B, et al. Diversity of plasmids and genes encoding resistance to extended spectrum cephalosporins in commensal escherichia coli from dutch livestock in 2007–2017. Front Microbiol. 2019;10. https://doi.org/10.3389/fmicb.2019.00076Auffret MD, Dewhurst RJ, Duthie CA, Rooke JA, John Wallace R, Freeman TC, et al. The rumen microbiome as a reservoir of antimicrobial resistance and pathogenicity genes is directly affected by diet in beef cattle. Microbiome. 2017;5:159. https://doi.org/10.1186/s40168-017-0378-zArticle 

    Google Scholar 
    Sabino YNV, Santana MF, Oyama LB, Santos FG, Moreira AJS, Huws SA, et al. Characterization of antibiotic resistance genes in the species of the rumen microbiota. Nat Commun. 2019;10:5252. https://doi.org/10.1038/s41467-019-13118-0Article 
    CAS 

    Google Scholar 
    Brown Kav A, Benhar I, Mizrahi I. Rumen plasmids. In: Gophna U, editor. Lateral gene transfer in evolution. New York, NY: Springer New York; 2013. p. 105–20.Mizrahi I, Wallace RJ, Moraïs S. The rumen microbiome: balancing food security and environmental impacts. Nat Rev Microbiol. 2021;19:553–66. https://doi.org/10.1038/s41579-021-00543-6Article 
    CAS 

    Google Scholar 
    Dionisio F, Zilhão R, Gama JA. Interactions between plasmids and other mobile genetic elements affect their transmission and persistence. Plasmid. 2019;102:29–36. https://doi.org/10.1016/j.plasmid.2019.01.003Article 
    CAS 

    Google Scholar 
    Brown Kav A, Sasson G, Jami E, Doron-Faigenboim A, Benhar I, Mizrahi I. Insights into the bovine rumen plasmidome. Proc Natl Acad Sci USA. 2012;109:5452–7. https://doi.org/10.1073/pnas.1116410109Article 

    Google Scholar 
    Kav AB, Rozov R, Bogumil D, Sørensen SJ, Hansen LH, Benhar I, et al. Unravelling plasmidome distribution and interaction with its hosting microbiome. Environ Microbiol. 2020;22:32–44. https://doi.org/10.1111/1462-2920.14813Article 

    Google Scholar 
    Jørgensen TS, Xu Z, Hansen MA, Sørensen SJ, Hansen LH. Hundreds of circular novel plasmids and DNA elements identified in a rat cecum metamobilome. PLoS One. 2014;9:e87924. https://doi.org/10.1371/journal.pone.0087924Article 
    CAS 

    Google Scholar 
    He Q, Pilosof S, Tiedje KE, Ruybal-Pesántez S, Artzy-Randrup Y, Baskerville EB, et al. Networks of genetic similarity reveal non-neutral processes shape strain structure in Plasmodium falciparum. Nat Commun. 2018;9:1817. https://doi.org/10.1038/s41467-018-04219-3Article 
    CAS 

    Google Scholar 
    Acman M, van Dorp L, Santini JM, Balloux F. Large-scale network analysis captures biological features of bacterial plasmids. Nat Commun. 2020;11:2452. https://doi.org/10.1038/s41467-020-16282-wArticle 
    CAS 

    Google Scholar 
    Redondo-Salvo S, Fernández-López R, Ruiz R, Vielva L, de Toro M, Rocha EPC, et al. Pathways for horizontal gene transfer in bacteria revealed by a global map of their plasmids. Nat Commun. 2020;11:3602. https://doi.org/10.1038/s41467-020-17278-2Article 
    CAS 

    Google Scholar 
    Savary P, Foltête JC, Moal H, Vuidel G, Garnier S. Analysing landscape effects on dispersal networks and gene flow with genetic graphs. Mol Ecol Resour. 2021;21:1167–85. https://doi.org/10.1111/1755-0998.13333Article 

    Google Scholar 
    Pilosof S, He Q, Tiedje KE, Ruybal-Pesántez S, Day KP, Pascual M. Competition for hosts modulates vast antigenic diversity to generate persistent strain structure in Plasmodium falciparum. PLoS Biol. 2019;17:e3000336. https://doi.org/10.1371/journal.pbio.3000336Article 
    CAS 

    Google Scholar 
    Brilli M, Mengoni A, Fondi M, Bazzicalupo M, Liò P, Fani R. Analysis of plasmid genes by phylogenetic profiling and visualization of homology relationships using Blast2Network. BMC Bioinform. 2008;9:551. https://doi.org/10.1186/1471-2105-9-551Article 
    CAS 

    Google Scholar 
    Fondi M, Karkman A, Tamminen MV, Bosi E, Virta M, Fani R, et al. “Every gene is everywhere but the environment selects”: global geolocalization of gene sharing in environmental samples through network analysis. Genome Biol Evol. 2016;8:1388–1400. https://doi.org/10.1093/gbe/evw077Article 

    Google Scholar 
    Tamminen M, Virta M, Fani R, Fondi M. Large-scale analysis of plasmid relationships through gene-sharing networks. Mol Biol Evol. 2012;29:1225–40. https://doi.org/10.1093/molbev/msr292Article 
    CAS 

    Google Scholar 
    Yamashita A, Sekizuka T, Kuroda M. Characterization of antimicrobial resistance dissemination across plasmid communities classified by network analysis. Pathogens. 2014;3:356–76. https://doi.org/10.3390/pathogens3020356Article 
    CAS 

    Google Scholar 
    Pastor-Satorras R, Castellano C, Van Mieghem P, Vespignani A. Epidemic processes in complex networks. Rev Mod Phys. 2015;87:925–79. https://doi.org/10.1103/RevModPhys.87.925Article 

    Google Scholar 
    Pilosof S, Morand S, Krasnov BR, Nunn CL. Potential parasite transmission in multi-host networks based on parasite sharing. PLoS One. 2015;10:e0117909 https://doi.org/10.1371/journal.pone.0117909Article 
    CAS 

    Google Scholar 
    VanderWaal KL, Atwill ER, Isbell LA, McCowan B.Linking social and pathogen transmission networks using microbial genetics in giraffe (Giraffa camelopardalis).J Anim Ecol.2014;83:406–14. https://doi.org/10.1111/1365-2656.12137Article 

    Google Scholar 
    Kauffman K, Werner CS, Titcomb G, Pender M, Rabezara JY, Herrera JP, et al. Comparing transmission potential networks based on social network surveys, close contacts and environmental overlap in rural Madagascar. J R Soc Interface. 2022;19:20210690. https://doi.org/10.1098/rsif.2021.0690Article 

    Google Scholar 
    Dallas TA, Han BA, Nunn CL, Park AW, Stephens PR, Drake JM. Host traits associated with species roles in parasite sharing networks. Oikos. 2019;128:23–32. https://doi.org/10.1111/oik.05602Article 

    Google Scholar 
    Matlock W, Chau KK, AbuOun M, Stubberfield E, Barker L, Kavanagh J, et al. Genomic network analysis of environmental and livestock F-type plasmid populations. ISME J. 2021;15:2322–35. https://doi.org/10.1038/s41396-021-00926-wArticle 
    CAS 

    Google Scholar 
    Pilosof S, Porter MA, Pascual M, Kéfi S. The multilayer nature of ecological networks. Nat Ecol Evol. 2017;1:0101. https://doi.org/10.1038/s41559-017-0101Article 

    Google Scholar 
    Paull SH, Song S, McClure KM, Sackett LC, Kilpatrick AM, Johnson PTJ. From superspreaders to disease hotspots: linking transmission across hosts and space. Front Ecol Environ. 2012;10:75–82. https://doi.org/10.1890/110111Article 

    Google Scholar 
    Hutchinson MC, Bramon Mora B, Pilosof S, Barner AK, Kéfi S, Thébault E, et al. Seeing the forest for the trees: putting multilayer networks to work for community ecology. Funct Ecol. 2019;33:206–17. https://doi.org/10.1111/1365-2435.13237Article 

    Google Scholar 
    Kivelä M, Arenas A, Barthelemy M, Gleeson JP, Moreno Y, Porter MA. Multilayer networks. J Complex Netw. 2014;2:203–71. https://doi.org/10.1093/comnet/cnu016Article 

    Google Scholar 
    Lloyd-Smith JO, Schreiber SJ, Kopp PE, Getz WM. Superspreading and the effect of individual variation on disease emergence. Nature. 2005;438:355–9. https://doi.org/10.1038/nature04153Article 
    CAS 

    Google Scholar 
    Fortuna MA, Popa-Lisseanu AG, Ibáñez C, Bascompte J. The roosting spatial network of a bird-predator bat. Ecology. 2009;90:934–44. https://doi.org/10.1890/08-0174.1Article 

    Google Scholar 
    Newman MEJ, Girvan M. Finding and evaluating community structure in networks. Phys Rev E Stat Nonlin Soft Matter Phys. 2004;69:026113. https://doi.org/10.1103/PhysRevE.69.026113Article 
    CAS 

    Google Scholar 
    Rosvall M, Bergstrom CT. Maps of random walks on complex networks reveal community structure. Proc Natl Acad Sci USA. 2008;105:1118–23. https://doi.org/10.1073/pnas.0706851105Article 

    Google Scholar 
    De Domenico M, Lancichinetti A, Arenas A, Rosvall M. Identifying modular flows on multilayer networks reveals highly overlapping organization in interconnected systems. Phys Rev X. 2015;5:011027. https://doi.org/10.1103/PhysRevX.5.011027Article 
    CAS 

    Google Scholar 
    Farage C, Edler D, Eklöf A, Rosvall M, Pilosof S. Identifying flow modules in ecological networks using Infomap. Methods Ecol Evol. 2021;12:778–86. https://doi.org/10.1111/2041-210x.13569Article 

    Google Scholar 
    Popa O, Hazkani-Covo E, Landan G, Martin W, Dagan T. Directed networks reveal genomic barriers and DNA repair bypasses to lateral gene transfer among prokaryotes. Genome Res. 2011;21:599–609. https://doi.org/10.1101/gr.115592.110Article 
    CAS 

    Google Scholar 
    Smillie C, Garcillán-Barcia MP, Francia MV, Rocha EPC, de la Cruz F. Mobility of plasmids. Microbiol Mol Biol Rev. 2010;74:434–52. https://doi.org/10.1128/MMBR.00020-10Article 
    CAS 

    Google Scholar 
    Garcillán-Barcia MP, Francia MV, de la Cruz F. The diversity of conjugative relaxases and its application in plasmid classification. FEMS Microbiol Rev. 2009;33:657–87. https://doi.org/10.1111/j.1574-6976.2009.00168.xArticle 
    CAS 

    Google Scholar 
    Coluzzi C, Guédon G, Devignes MD, Ambroset C, Loux V, Lacroix T, et al. A glimpse into the world of integrative and mobilizable elements in streptococci reveals an unexpected diversity and novel families of mobilization proteins. Front Microbiol. 2017;8:443. https://doi.org/10.3389/fmicb.2017.00443Article 

    Google Scholar 
    Moraïs S, Mizrahi I. Islands in the stream: from individual to communal fiber degradation in the rumen ecosystem. FEMS Microbiol Rev. 2019;43:362–79. https://doi.org/10.1093/femsre/fuz007Article 
    CAS 

    Google Scholar 
    León-Sampedro R, DelaFuente J, Díaz-Agero C, Crellen T, Musicha P, Rodríguez-Beltrán J, et al. Pervasive transmission of a carbapenem resistance plasmid in the gut microbiota of hospitalized patients. Nat Microbiol. 2021;6:606–16. https://doi.org/10.1038/s41564-021-00879-yArticle 
    CAS 

    Google Scholar 
    Rocha LEC, Singh V, Esch M, Lenaerts T, Liljeros F, Thorson A. Dynamic contact networks of patients and MRSA spread in hospitals. Sci Rep. 2020;10:9336. https://doi.org/10.1038/s41598-020-66270-9Article 
    CAS 

    Google Scholar 
    Lerner A, Adler A, Abu-Hanna J, Cohen Percia S, Kazma Matalon M, Carmeli Y. Spread of KPC-producing carbapenem-resistant Enterobacteriaceae: the importance of super-spreaders and rectal KPC concentration. Clin Microbiol Infect. 2015;21:470.e1–7. https://doi.org/10.1016/j.cmi.2014.12.015Article 
    CAS 

    Google Scholar 
    Stein RA, Katz DE. Escherichia coli, cattle and the propagation of disease. FEMS Microbiol Lett. 2017;364. https://doi.org/10.1093/femsle/fnx050.de Freslon I, Martínez-López B, Belkhiria J, Strappini A, Monti G. Use of social network analysis to improve the understanding of social behaviour in dairy cattle and its impact on disease transmission. Appl Anim Behav Sci. 2019;213:47–54. https://doi.org/10.1016/j.applanim.2019.01.006Article 

    Google Scholar 
    Rushmore J, Caillaud D, Hall RJ, Stumpf RM, Meyers LA, Altizer S. Network-based vaccination improves prospects for disease control in wild chimpanzees. J R Soc Interface. 2014;11:20140349. https://doi.org/10.1098/rsif.2014.0349Article 

    Google Scholar 
    Xue H, Cordero OX, Camas FM, Trimble W, Meyer F, Guglielmini J, et al. Eco-evolutionary dynamics of episomes among ecologically cohesive bacterial populations. MBio. 2015;6:e00552–15. https://doi.org/10.1128/mBio.00552-15Article 
    CAS 

    Google Scholar 
    Evans DR, Griffith MP, Sundermann AJ, Shutt KA, Saul MI, Mustapha MM, et al. Systematic detection of horizontal gene transfer across genera among multidrug-resistant bacteria in a single hospital. Elife. 2020;9. https://doi.org/10.7554/eLife.53886Abe R, Oyama F, Akeda Y, Nozaki M, Hatachi T, Okamoto Y, et al. Hospital-wide outbreaks of carbapenem-resistant Enterobacteriaceae horizontally spread through a clonal plasmid harbouring bla IMP-1 in children’s hospitals in Japan. J Antimicrob Chemother. 2021;76:3314–7.Article 
    CAS 

    Google Scholar 
    Bingen EH, Desjardins P, Arlet G, Bourgeois F, Mariani-Kurkdjian P, Lambert-Zechovsky NY, et al. Molecular epidemiology of plasmid spread among extended broad-spectrum beta-lactamase-producing Klebsiella pneumoniae isolates in a pediatric hospital. J Clin Microbiol. 1993;31:179–84. https://doi.org/10.1128/jcm.31.2.179-184.1993.Bai H, He LY, Wu DL, Gao FZ, Zhang M, Zou HY, et al. Spread of airborne antibiotic resistance from animal farms to the environment: dispersal pattern and exposure risk. Environ Int. 2022;158:106927 https://doi.org/10.1016/j.envint.2021.106927Article 
    CAS 

    Google Scholar 
    Boyland NK, Mlynski DT, James R, Brent LJN, Croft DP. The social network structure of a dynamic group of dairy cows: from individual to group level patterns. Appl Anim Behav Sci. 2016;174:1–10. https://doi.org/10.1016/j.applanim.2015.11.016Article 

    Google Scholar 
    Björk JR, Dasari M, Grieneisen L, Archie EA. Primate microbiomes over time: longitudinal answers to standing questions in microbiome research. Am J Primatol. 2019;81:e22970. https://doi.org/10.1002/ajp.22970Article 

    Google Scholar 
    Dib JR, Wagenknecht M, Farías ME, Meinhardt F. Strategies and approaches in plasmidome studies—uncovering plasmid diversity disregarding of linear elements? Front Microbiol. 2015;6. https://doi.org/10.3389/fmicb.2015.00463Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19:455–77. https://doi.org/10.1089/cmb.2012.0021Article 
    CAS 

    Google Scholar 
    Rozov R, Brown Kav A, Bogumil D, Shterzer N, Halperin E, Mizrahi I, et al. Recycler: an algorithm for detecting plasmids from de novo assembly graphs. Bioinformatics. 2017;33:475–82. https://doi.org/10.1093/bioinformatics/btw651Article 
    CAS 

    Google Scholar 
    Orlek A, Stoesser N, Anjum MF, Doumith M, Ellington MJ, Peto T, et al. Plasmid classification in an era of whole-genome sequencing: application in studies of antibiotic resistance epidemiology. Front Microbiol. 2017;8:182. https://doi.org/10.3389/fmicb.2017.00182Article 

    Google Scholar 
    Komsta L, Novomestky F. Moments, cumulants, skewness, kurtosis and related tests. R package version. 2015;14.Rosvall M, Axelsson D, Bergstrom CT. The map equation. Eur Phys J Spec Top. 2010;178:13–23. https://doi.org/10.1140/epjst/e2010-01179-1Article 

    Google Scholar 
    Bascompte J, Jordano P, Melián CJ, Olesen JM. The nested assembly of plant–animal mutualistic networks. Proc Natl Acad Sci USA. 2003;100:9383–7. https://doi.org/10.1073/pnas.1633576100Article 
    CAS 

    Google Scholar 
    Vázquez DP, Poulin R, Krasnov BR, Shenbrot GI. Species abundance and the distribution of specialization in host–parasite interaction networks. J Anim Ecol. 2005;74:946–55.Article 

    Google Scholar 
    Fortuna MA, Stouffer DB, Olesen JM, Jordano P, Mouillot D, Krasnov BR, et al. Nestedness versus modularity in ecological networks: two sides of the same coin? J Anim Ecol. 2010;79:811–7. https://doi.org/10.1111/j.1365-2656.2010.01688.xArticle 

    Google Scholar 
    Gillespie DT. Exact stochastic simulation of coupled chemical reactions. J Phys Chem. 1977;81:2340–61. https://doi.org/10.1021/j100540a008Article 
    CAS 

    Google Scholar 
    R Core Team. R: a language and environment for statistical computing; 2021. More