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    Early Mars habitability and global cooling by H2-based methanogens

    Cockell, C. S. et al. Habitability: a review. Astrobiology 16, 89–117 (2016).ADS 
    Article 

    Google Scholar 
    Michalski, J. R. et al. The Martian subsurface as a potential window into the origin of life. Nat. Geosci. 11, 21–26 (2018).ADS 
    Article 

    Google Scholar 
    Fairén, A. G. et al. Stability against freezing of aqueous solutions on early Mars. Nature 459, 401–404 (2009).ADS 
    Article 

    Google Scholar 
    Clifford, S. M. et al. Depth of the Martian cryosphere: Revised estimates and implications for the existence and detection of subpermafrost groundwater. J. Geophys. Res. 115, E07001 (2010).ADS 
    Article 

    Google Scholar 
    Rivera-Valentín, E. G., Chevrier, V. F., Soto, A. & Martínez, G. Distribution and habitability of (meta)stable brines on present-day Mars. Nat. Astron. 4, 756–761 (2020).ADS 
    Article 

    Google Scholar 
    Stevens, A. H., Patel, M. R. & Lewis, S. R. Numerical modelling of the transport of trace gases including methane in the subsurface of Mars. Icarus 250, 587–594 (2015).ADS 
    Article 

    Google Scholar 
    Sholes, S. F., Krissansen-Totton, J. & Catling, D. C. A maximum subsurface biomass on mars from untapped free energy: CO and H2 as potential antibiosignatures. Astrobiology 19, 655–668 (2019).ADS 
    Article 

    Google Scholar 
    Wordsworth, R. D. The climate of early Mars. Annu. Rev. Earth Planet. Sci. 44, 381–408 (2016).ADS 
    Article 

    Google Scholar 
    Liu, J. et al. Anoxic chemical weathering under a reducing greenhouse on early Mars. Nat. Astron. 5, 503–509 (2021).ADS 
    Article 

    Google Scholar 
    Battistuzzi, F. U., Feijao, A. & Hedges, S. B. A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land. BMC Evol. Biol. 4, 44 (2004).Article 

    Google Scholar 
    Martin, W. F. & Sousa, F. L. Early microbial evolution: the age of anaerobes. Cold Spring Harbor Perspect. Biol 8, a018127 (2016).Article 

    Google Scholar 
    Sauterey, B. et al. Co-evolution of primitive methane-cycling ecosystems and early Earth’s atmosphere and climate. Nat. Commun. 11, 2705 (2020).ADS 
    Article 

    Google Scholar 
    Affholder, A. et al. Bayesian analysis of Enceladus’s plume data to assess methanogenesis. Nat. Astron. 5, 805–814 (2021).ADS 
    Article 

    Google Scholar 
    Wordsworth, R. et al. Transient reducing greenhouse warming on early Mars. Geophys. Res. Lett. 44, 665–671 (2017).ADS 
    Article 

    Google Scholar 
    Turbet, M., Boulet, C. & Karman, T. Measurements and semi-empirical calculations of CO2 + CH4 and CO2 + H2 collision-induced absorption across a wide range of wavelengths and temperatures. Application for the prediction of early Mars surface temperature. Icarus 346, 113762 (2020).Article 

    Google Scholar 
    Price, P. B. & Sowers, T. Temperature dependence of metabolic rates for microbial growth, maintenance, and survival. Proc. Nat. Acad. Sci. USA 101, 4631–4636 (2004).ADS 
    Article 

    Google Scholar 
    Taubner, R.-S. et al. Biological methane production under putative Enceladus-like conditions. Nat. Commun. 9, 748 (2018).ADS 
    Article 

    Google Scholar 
    Ramirez, R. M. A warmer and wetter solution for early Mars and the challenges with transient warming. Icarus 297, 71–82 (2017).ADS 
    Article 

    Google Scholar 
    Kharecha, P., Kasting, J. & Siefert, J. A coupled atmosphere–ecosystem model of the early Archean Earth. Geobiology 3, 53–76 (2005).Article 

    Google Scholar 
    Tarnas, J. D. et al. Radiolytic H2 production on Noachian Mars: implications for habitability and atmospheric warming. Earth Planet. Sci. Lett. 502, 133–145 (2018).ADS 
    Article 

    Google Scholar 
    Yung, Y. L. et al. Methane on Mars and habitability: challenges and responses. Astrobiology 18, 1221–1242 (2018).ADS 
    Article 

    Google Scholar 
    Knutsen, E. W. et al. Comprehensive investigation of Mars methane and organics with ExoMars/NOMAD. Icarus 357, 114266 (2021).Article 

    Google Scholar 
    Cockell, C. S. Trajectories of martian habitability. Astrobiology 14, 182–203 (2014).ADS 
    Article 

    Google Scholar 
    Westall, F. et al. Biosignatures on Mars: What, where, and how? Implications for the search for Martian life. Astrobiology 15, 998–1029 (2015).ADS 
    Article 

    Google Scholar 
    Lepot, K. Signatures of early microbial life from the Archean (4 to 2.5 Ga) eon. Earth Sci. Rev. 209, 103296 (2020).Article 

    Google Scholar 
    Fastook, J. L. & Head, J. W. Glaciation in the late noachian icy highlands: Ice accumulation, distribution, flow rates, basal melting, and top-down melting rates and patterns. Planet. Space Sci. 106, 82–98 (2015).ADS 
    Article 

    Google Scholar 
    Fassett, C. I. & Head, J. W. Valley network-fed, open-basin lakes on Mars: distribution and implications for Noachian surface and subsurface hydrology. Icarus 198, 37–56 (2008).ADS 
    Article 

    Google Scholar 
    Tanaka, K. L. et al. Geologic Map of Mars: U.S. Geological Survey Scientific Investigations Map 3292, Scale 1000,000 (US Geological Survey, 2014); https://doi.org/10.3133/sim3292Sun, V. Z. & Stack, K. M. Geologic Map of Jezero Crater and the Nili Planum Region, Mars: U.S. Geological Survey Scientific Investigations Map 3464, Scale 1000 (US Geological Survey, 2020); https://doi.org/10.3133/sim3464Ward, P. The Medea Hypothesis (Princeton Univ. Press, 2009).Chopra, A. & Lineweaver, C. H. The Case for a Gaian bottleneck: the biology of habitability. Astrobiology 16, 7–22 (2016).ADS 
    Article 

    Google Scholar 
    Arney, G. et al. The Pale Orange Dot: The Spectrum and Habitability of Hazy Archean Earth. Astrobiology 16, 873–899 (2016).Batalha, N. et al. Testing the early Mars H2-CO2 greenhouse hypothesis with a 1-D photochemical model. Icarus 258, 337–349 (2015).ADS 
    Article 

    Google Scholar 
    Stüeken, E. E. et al. Isotopic evidence for biological nitrogen fixation by molybdenum-nitrogenase from 3.2 Gyr. Nature 520, 666–669 (2015).ADS 
    Article 

    Google Scholar 
    Cockell, C. S. et al. Minimum units of habitability and their abundance in the universe. Astrobiology 21, 481–489 (2021).ADS 
    Article 

    Google Scholar 
    Adams, D. et al. Nitrogen fixation at early Mars. Astrobiology 21, 968–980 (2021).ADS 
    Article 

    Google Scholar 
    Fergason, R. L., Hare, T. M. and Laura, J. HRSC and MOLA Blended Digital Elevation Model at 200m v2. Astrogeology PDS Annex (US Geological Survey, 2018); http://bit.ly/HRSC_MOLA_Blend_v0Sauterey, B. MarsEcosys v.1.0. Zenodo https://doi.org/10.5281/zenodo.6963348 (2022). More

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    Resolving malaria’s dry-season dilemma

    Seasonal fluctuations in animal population dynamics are among the most fundamental attributes of life on Earth. A long recognized but poorly understood example is the dramatic seasonal fluctuation in the abundance of malaria vectors in the semi-arid savannah and Sahel regions of Africa. In these regions, the vector mosquitoes largely disappear during a prolonged 3- to 8-month dry season, when lack of rain causes the aquatic larval habitats to disappear. As a result, malaria transmission plummets. When the rains return, the mosquito vectors rapidly reappear, leading to a resurgence of malaria transmission. How the vector populations are able to persist through the prolonged dry season and rapidly rebound with the onset of rains is referred to as the ‘dry-season malaria paradox’, and has remained an enduring mystery of malariology for nearly 100 years. Writing in Nature Ecology & Evolution, Faiman et al.1 help to resolve this mystery by using an innovative isotopic labelling strategy: they demonstrate that at least approximately 20% of the local population of the malaria vector Anopheles coluzzi in the West African Sahel survive the dry season locally by undergoing summer dormancy, known as aestivation. More

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    Inter-annual variability patterns of reef cryptobiota in the central Red Sea across a shelf gradient

    Knowlton, N. et al. in Life in the World’s Oceans 65–78 (Wiley-Blackwell, 2010).Fisher, R. et al. Species richness on coral reefs and the pursuit of convergent global estimates. Curr. Biol. 25, 500–505. https://doi.org/10.1016/j.cub.2014.12.022 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    Brandl, S. J., Goatley, C. H. R., Bellwood, D. R. & Tornabene, L. The hidden half: Ecology and evolution of cryptobenthic fishes on coral reefs. Biol. Rev. 93, 1846–1873. https://doi.org/10.1111/brv.12423 (2018).Article 
    PubMed 

    Google Scholar 
    Appeltans, W. et al. The magnitude of global marine species diversity. Curr. Biol. 22, 2189–2202. https://doi.org/10.1016/j.cub.2012.09.036 (2012).CAS 
    Article 
    PubMed 

    Google Scholar 
    Carvalho, S. et al. Beyond the visual: Using metabarcoding to characterize the hidden reef cryptobiome. Proc. R. Soc. B Biol. Sci. https://doi.org/10.1098/rspb.2018.2697 (2019).Article 

    Google Scholar 
    Kramer, M. J., Bellwood, O., Fulton, C. J. & Bellwood, D. R. Refining the invertivore: Diversity and specialisation in fish predation on coral reef crustaceans. Mar. Biol. 162, 1779–1786. https://doi.org/10.1007/s00227-015-2710-0 (2015).CAS 
    Article 

    Google Scholar 
    Brandl, S. J. et al. Demographic dynamics of the smallest marine vertebrates fuel coral reef ecosystem functioning. Science 364, 1189–1192. https://doi.org/10.1126/science.aav3384 (2019).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Kramer, M. J., Bellwood, D. R. & Bellwood, O. Cryptofauna of the epilithic algal matrix on an inshore coral reef, Great Barrier Reef. Coral Reefs 31, 1007–1015. https://doi.org/10.1007/s00338-012-0924-x (2012).ADS 
    Article 

    Google Scholar 
    Rocha, L. A. et al. Specimen collection: An essential tool. Science 344, 814–815. https://doi.org/10.1126/science.344.6186.814 (2014).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Berumen, M. L. et al. The status of coral reef ecology research in the Red Sea. Coral Reefs 32, 737–748. https://doi.org/10.1007/s00338-013-1055-8 (2013).ADS 
    Article 

    Google Scholar 
    Paknia, O., Sh, H. R. & Koch, A. Lack of well-maintained natural history collections and taxonomists in megadiverse developing countries hampers global biodiversity exploration. Org. Divers. Evol. 15, 619–629. https://doi.org/10.1007/s13127-015-0202-1 (2015).Article 

    Google Scholar 
    Knowlton, N. & Leray, M. Censusing marine life in the twentyfirst Century. Genome 58, 238–238 (2015).
    Google Scholar 
    Yu, D. W. et al. Biodiversity soup: Metabarcoding of arthropods for rapid biodiversity assessment and biomonitoring. Methods Ecol. Evol. 3, 613–623. https://doi.org/10.1111/j.2041-210X.2012.00198.x (2012).Article 

    Google Scholar 
    Ransome, E. et al. The importance of standardization for biodiversity comparisons: A case study using autonomous reef monitoring structures (ARMS) and metabarcoding to measure cryptic diversity on Mo’orea coral reefs, French Polynesia. PLoS ONE https://doi.org/10.1371/journal.pone.0175066 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Coker, D. J., DiBattista, J. D., Sinclair-Taylor, T. H. & Berumen, M. L. Spatial patterns of cryptobenthic coral-reef fishes in the Red Sea. Coral Reefs 37, 193–199. https://doi.org/10.1007/s00338-017-1647-9 (2018).ADS 
    Article 

    Google Scholar 
    Pearman, J. K. et al. Cross-shelf investigation of coral reef cryptic benthic organisms reveals diversity patterns of the hidden majority. Sci. Rep. 8, 8090. https://doi.org/10.1038/s41598-018-26332-5 (2018).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Pearman, J. K. et al. Disentangling the complex microbial community of coral reefs using standardized Autonomous Reef Monitoring Structures (ARMS). Mol. Ecol. 28, 3496–3507. https://doi.org/10.1111/mec.15167 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Selkoe, K. A. et al. The DNA of coral reef biodiversity: Predicting and protecting genetic diversity of reef assemblages. Proc. R. Soc. B-Biol. Sci. https://doi.org/10.1098/rspb.2016.0354 (2016).Article 

    Google Scholar 
    DiBattista, J. D. et al. Digging for DNA at depth: Rapid universal metabarcoding surveys (RUMS) as a tool to detect coral reef biodiversity across a depth gradient. PeerJ https://doi.org/10.7717/peerj.6379 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    DiBattista, J. D. et al. Assessing the utility of eDNA as a tool to survey reef-fish communities in the Red Sea. Coral Reefs 36, 1245–1252. https://doi.org/10.1007/s00338-017-1618-1 (2017).ADS 
    Article 

    Google Scholar 
    Nester, G. M. et al. Development and evaluation of fish eDNA metabarcoding assays facilitate the detection of cryptic seahorse taxa (family: Syngnathidae). Environ. DNA 2, 614–626 (2020).Article 

    Google Scholar 
    West, K. M. et al. eDNA metabarcoding survey reveals fine-scale coral reef community variation across a remote, tropical island ecosystem. Mol. Ecol. 29, 1069–1086. https://doi.org/10.1111/mec.15382 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    DiBattista, J. D. et al. Environmental DNA can act as a biodiversity barometer of anthropogenic pressures in coastal ecosystems. Sci. Rep. https://doi.org/10.1038/s41598-020-64858-9 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Worm, B. et al. Impacts of biodiversity loss on ocean ecosystem services. Science 314, 787–790. https://doi.org/10.1126/science.1132294 (2006).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Spalding, M. et al. Mapping the global value and distribution of coral reef tourism. Mar. Policy 82, 104–113. https://doi.org/10.1016/j.marpol.2017.05.014 (2017).Article 

    Google Scholar 
    Thomsen, P. F. & Willerslev, E. Environmental DNA – An emerging tool in conservation for monitoring past and present biodiversity. Biol. Cons. 183, 4–18. https://doi.org/10.1016/j.biocon.2014.11.019 (2015).Article 

    Google Scholar 
    Hughes, T. P. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80–83. https://doi.org/10.1126/science.aan8048 (2018).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Monroe, A. A. et al. In situ observations of coral bleaching in the central Saudi Arabian Red Sea during the 2015/2016 global coral bleaching event. PLoS ONE https://doi.org/10.1371/journal.pone.0195814 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Roth, F. et al. Coral reef degradation affects the potential for reef recovery after disturbance. Mar. Environ. Res. 142, 48–58. https://doi.org/10.1016/j.marenvres.2018.09.022 (2018).CAS 
    Article 
    PubMed 

    Google Scholar 
    Foster, T. & Gilmour, J. P. Seeing red: Coral larvae are attracted to healthy-looking reefs. Mar. Ecol. Prog. Ser. 559, 65–71. https://doi.org/10.3354/meps11902 (2016).ADS 
    CAS 
    Article 

    Google Scholar 
    Karcher, D. B. et al. Nitrogen eutrophication particularly promotes turf algae in coral reefs of the central Red Sea. PeerJ https://doi.org/10.7717/peerj.8737 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Pancrazi, I., Ahmed, H., Cerrano, C. & Montefalcone, M. Synergic effect of global thermal anomalies and local dredging activities on coral reefs of the Maldives. Marine Pollut. Bull. https://doi.org/10.1016/j.marpolbul.2020.111585 (2020).Article 

    Google Scholar 
    Vercelloni, J. et al. Forecasting intensifying disturbance effects on coral reefs. Glob. Change Biol. 26, 2785–2797. https://doi.org/10.1111/gcb.15059 (2020).ADS 
    Article 

    Google Scholar 
    González-Barrios, F. J., Cabral-Tena, R. A. & Alvarez-Filip, L. Recovery disparity between coral cover and the physical functionality of reefs with impaired coral assemblages. Glob. Change Biol. 27, 640–651. https://doi.org/10.1111/gcb.15431 (2020).ADS 
    Article 

    Google Scholar 
    Rice, M. M., Ezzat, L. & Burkepile, D. E. Corallivory in the anthropocene: Interactive effects of anthropogenic stressors and corallivory on coral reefs. Front. Marine Sci. https://doi.org/10.3389/fmars.2018.00525 (2019).Article 

    Google Scholar 
    Lin, Y.-J. et al. Long-term ecological changes in fishes and macro-invertebrates in the world’s warmest coral reefs. Sci. Total Environ. 750, 142254. https://doi.org/10.1016/j.scitotenv.2020.142254 (2021).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Loreau, M. & de Mazancourt, C. Biodiversity and ecosystem stability: A synthesis of underlying mechanisms. Ecol. Lett. 16, 106–115. https://doi.org/10.1111/ele.12073 (2013).Article 
    PubMed 

    Google Scholar 
    Cardinale, B. J. et al. Biodiversity loss and its impact on humanity. Nature 486, 59–67. https://doi.org/10.1038/nature11148 (2012).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Handley, L. L. How will the “molecular revolution’ contribute to biological recording?. Biol. J. Lin. Soc. 115, 750–766. https://doi.org/10.1111/bij.12516 (2015).Article 

    Google Scholar 
    Ducklow, H. W., Doney, S. C. & Steinberg, D. K. Contributions of long-term research and time-series observations to marine ecology and biogeochemistry. Ann. Rev. Mar. Sci. 1, 279–302. https://doi.org/10.1146/annurev.marine.010908.163801 (2009).Article 
    PubMed 

    Google Scholar 
    Hughes, B. B. et al. Long-term studies contribute disproportionately to ecology and policy. Bioscience 67, 271–281. https://doi.org/10.1093/biosci/biw185 (2017).Article 

    Google Scholar 
    Kraft, N. J. B. et al. Community assembly, coexistence and the environmental filtering metaphor. Funct. Ecol. 29, 592–599. https://doi.org/10.1111/1365-2435.12345 (2015).Article 

    Google Scholar 
    Leibold, M. A. et al. The metacommunity concept: A framework for multi-scale community ecology. Ecol. Lett. 7, 601–613. https://doi.org/10.1111/j.1461-0248.2004.00608.x (2004).Article 

    Google Scholar 
    Vellend, M. The Theory of Ecological Communities (MPB-57). (Princeton University Press, 2016).Condon, R. H. et al. Recurrent jellyfish blooms are a consequence of global oscillations. Proc. Natl. Acad. Sci. U.S.A. 110, 1000–1005. https://doi.org/10.1073/pnas.1210920110 (2013).ADS 
    Article 
    PubMed 

    Google Scholar 
    Boero, F., Kraberg, A. C., Krause, G. & Wiltshire, K. H. Time is an affliction: Why ecology cannot be as predictive as physics and why it needs time series. J. Sea Res. 101, 12–18. https://doi.org/10.1016/j.seares.2014.07.008 (2015).ADS 
    Article 

    Google Scholar 
    Pearman, J. K., Anlauf, H., Irigoien, X. & Carvalho, S. Please mind the gap – Visual census and cryptic biodiversity assessment at central Red Sea coral reefs. Mar. Environ. Res. 118, 20–30. https://doi.org/10.1016/j.marenvres.2016.04.011 (2016).CAS 
    Article 
    PubMed 

    Google Scholar 
    David, R. et al. Lessons from photo analyses of autonomous reef monitoring structures as tools to detect (bio-)geographical, spatial, and environmental effects. Mar. Pollut. Bull. 141, 420–429. https://doi.org/10.1016/j.marpolbul.2019.02.066 (2019).CAS 
    Article 
    PubMed 

    Google Scholar 
    Pennesi, C. & Danovaro, R. Assessing marine environmental status through microphytobenthos assemblages colonizing the autonomous reef monitoring structures (ARMS) and their potential in coastal marine restoration. Mar. Pollut. Bull. 125, 56–65. https://doi.org/10.1016/j.marpolbul.2017.08.001 (2017).CAS 
    Article 
    PubMed 

    Google Scholar 
    Chang, J. J. M., Ip, Y. C. A., Bauman, A. G. & Huang, D. MinION-in-ARMS: Nanopore sequencing to expedite barcoding of specimen-rich macrofaunal samples from Autonomous Reef Monitoring Structures. Front. Marine Sci. https://doi.org/10.3389/fmars.2020.00448 (2020).Article 

    Google Scholar 
    Hazeri, G. et al. Latitudinal species diversity and density of cryptic crustacean (Brachyura and Anomura) in micro-habitat Autonomous Reef Monitoring Structures across Kepulauan Seribu, Indonesia. Biodivers. J. Biol. Divers. 20 (2019).Al-Rshaidat, M. M. D. et al. Deep COI sequencing of standardized benthic samples unveils overlooked diversity of Jordanian coral reefs in the northern Red Sea. Genome 59, 724–737. https://doi.org/10.1139/gen-2015-0208 (2016).CAS 
    Article 
    PubMed 

    Google Scholar 
    Pearman, J. K. et al. Pan-regional marine benthic cryptobiome biodiversity patterns revealed by metabarcoding Autonomous Reef Monitoring Structures. Mol. Ecol. https://doi.org/10.1111/mec.15692 (2020).Article 
    PubMed 

    Google Scholar 
    Leray, M. & Knowlton, N. DNA barcoding and metabarcoding of standardized samples reveal patterns of marine benthic diversity. Proc. Natl. Acad. Sci. U.S.A. 112, 2076–2081. https://doi.org/10.1073/pnas.1424997112 (2015).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Obst, M. et al. A marine biodiversity observation network for genetic monitoring of hard-bottom communities (ARMS-MBON). Front. Marine Sci. https://doi.org/10.3389/fmars.2020.572680 (2020).Article 

    Google Scholar 
    Hughes, T. P. et al. Ecological memory modifies the cumulative impact of recurrent climate extremes. Nat. Clim. Chang. 9, 40–43. https://doi.org/10.1038/s41558-018-0351-2 (2019).ADS 
    Article 

    Google Scholar 
    Hughes, T. P., Kerry, J. T. & Simpson, T. Large-scale bleaching of corals on the Great Barrier Reef. Ecology 99, 501–501. https://doi.org/10.1002/ecy.2092 (2018).CAS 
    Article 
    PubMed 

    Google Scholar 
    Furby, K. A., Bouwmeester, J. & Berumen, M. L. Susceptibility of central Red Sea corals during a major bleaching event. Coral Reefs 32, 505–513. https://doi.org/10.1007/s00338-012-0998-5 (2013).ADS 
    Article 

    Google Scholar 
    Froehlich, C. Y. M., Klanten, O. S., Hing, M. L., Dowton, M. & Wong, M. Y. L. Uneven declines between corals and cryptobenthic fish symbionts from multiple disturbances. Sci. Rep. https://doi.org/10.1038/s41598-021-95778-x (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bellwood, D. R. et al. Coral recovery may not herald the return of fishes on damaged coral reefs. Oecologia 170, 567–573. https://doi.org/10.1007/s00442-012-2306-z (2012).ADS 
    Article 
    PubMed 

    Google Scholar 
    Archana, A. & Baker, D. M. Multifunctionality of an urbanized coastal marine ecosystem. Front. Marine Sci. https://doi.org/10.3389/fmars.2020.557145 (2020).Article 

    Google Scholar 
    Servis, J. A., Reid, B. N., Timmers, M. A., Stergioula, V. & Naro-Maciel, E. Characterizing coral reef biodiversity: Genetic species delimitation in brachyuran crabs of Palmyra Atoll Central Pacific. Mitochondrial DNA Part A 31, 178–189. https://doi.org/10.1080/24701394.2020.1769087 (2020).CAS 
    Article 

    Google Scholar 
    Chaves-Fonnegra, A. et al. Bleaching events regulate shifts from corals to excavating sponges in algae-dominated reefs. Glob. Change Biol. 24, 773–785. https://doi.org/10.1111/gcb.13962 (2018).ADS 
    Article 

    Google Scholar 
    Perry, C. T. & Morgan, K. M. Post-bleaching coral community change on southern Maldivian reefs: Is there potential for rapid recovery?. Coral Reefs 36, 1189–1194. https://doi.org/10.1007/s00338-017-1610-9 (2017).ADS 
    Article 

    Google Scholar 
    DeCarlo, T. M. The past century of coral bleaching in the Saudi Arabian central Red Sea. PeerJ https://doi.org/10.7717/peerj.10200 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Cortés, J. et al. in Coral Reefs of the Eastern Tropical Pacific: Persistence and Loss in a Dynamic Environment (eds Peter W. Glynn, Derek P. Manzello, & Ian C. Enochs) 203–250 (Springer Netherlands, 2017).Enochs, I. C. & Manzello, D. P. Species richness of motile cryptofauna across a gradient of reef framework erosion. Coral Reefs 31, 653–661. https://doi.org/10.1007/s00338-012-0886-z (2012).ADS 
    Article 

    Google Scholar 
    Timmers, M. A. et al. Biodiversity of coral reef cryptobiota shuffles but does not decline under the combined stressors of ocean warming and acidification. Proc. Natl. Acad. Sci. 118, e2103275118. https://doi.org/10.1073/pnas.2103275118 (2021).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Khalil, M. T., Bouwmeester, J. & Berumen, M. L. Spatial variation in coral reef fish and benthic communities in the central Saudi Arabian Red Sea. PeerJ https://doi.org/10.7717/peerj.3410 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Roik, A. et al. Year-long monitoring of physico-chemical and biological variables provide a comparative baseline of coral reef functioning in the central Red Sea. PLoS ONE https://doi.org/10.1371/journal.pone.0163939 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Largier, J. L. Considerations in estimating larval dispersal distances from oceanographic data. Ecol. Appl. 13, S71–S89 (2003).Article 

    Google Scholar 
    Volkov, I., Banavar, J. R., Hubbell, S. P. & Maritan, A. Patterns of relative species abundance in rainforests and coral reefs. Nature 450, 45–49. https://doi.org/10.1038/nature06197 (2007).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Alsaffar, Z., Cúrdia, J., Borja, A., Irigoien, X. & Carvalho, S. Consistent variability in beta-diversity patterns contrasts with changes in alpha-diversity along an onshore to offshore environmental gradient: The case of Red Sea soft-bottom macrobenthos. Mar. Biodivers. 49, 247–262. https://doi.org/10.1007/s12526-017-0791-3 (2017).Article 

    Google Scholar 
    Alsaffar, Z. et al. The role of seagrass vegetation and local environmental conditions in shaping benthic bacterial and macroinvertebrate communities in a tropical coastal lagoon. Sci. Rep. https://doi.org/10.1038/s41598-020-70318-1 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Rocha, L. A. et al. Mesophotic coral ecosystems are threatened and ecologically distinct from shallow water reefs. Science 361, 281–284. https://doi.org/10.1126/science.aaq1614 (2018).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Soininen, J., Lennon, J. J. & Hillebrand, H. A multivariate analysis of beta diversity across organisms and environments. Ecology 88, 2830–2838. https://doi.org/10.1890/06-1730.1 (2007).Article 
    PubMed 

    Google Scholar 
    Chust, G. et al. Dispersal similarly shapes both population genetics and community patterns in the marine realm. Sci. Rep. https://doi.org/10.1038/srep28730 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gianuca, A. T., Declerck, S. A. J., Lemmens, P. & De Meester, L. Effects of dispersal and environmental heterogeneity on the replacement and nestedness components of beta-diversity. Ecology 98, 525–533. https://doi.org/10.1002/ecy.1666 (2017).Article 
    PubMed 

    Google Scholar 
    Enochs, I. C., Toth, L. T., Brandtneris, V. W., Afflerbach, J. C. & Manzello, D. P. Environmental determinants of motile cryptofauna on an eastern Pacific coral reef. Mar. Ecol. Prog. Ser. 438, 105-U127. https://doi.org/10.3354/meps09259 (2011).ADS 
    Article 

    Google Scholar 
    Hughes, T. P. et al. Coral reefs in the anthropocene. Nature 546, 82–90. https://doi.org/10.1038/nature22901 (2017).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Fabricius, K. E. Effects of terrestrial runoff on the ecology of corals and coral reefs: Review and synthesis. Mar. Pollut. Bull. 50, 125–146. https://doi.org/10.1016/j.marpolbul.2004.11.028 (2005).CAS 
    Article 
    PubMed 

    Google Scholar 
    Chaidez, V., Dreano, D., Agusti, S., Duarte, C. M. & Hoteit, I. Decadal trends in Red Sea maximum surface temperature. Sci. Rep. https://doi.org/10.1038/s41598-018-25731-y (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Hubbell, S. P. in Monographs in Population Biology. The unified neutral theory of biodiversity and biogeography Vol. 32 Monographs in Population Biology i-xiv, 1–375 (2001).Dornelas, M., Connolly, S. R. & Hughes, T. P. Coral reef diversity refutes the neutral theory of biodiversity. Nature 440, 80–82. https://doi.org/10.1038/nature04534 (2006).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Baselga, A. Partitioning the turnover and nestedness components of beta diversity. Glob. Ecol. Biogeogr. 19, 134–143. https://doi.org/10.1111/j.1466-8238.2009.00490.x (2010).Article 

    Google Scholar 
    Legendre, P. Interpreting the replacement and richness difference components of beta diversity. Glob. Ecol. Biogeogr. 23, 1324–1334. https://doi.org/10.1111/geb.12207 (2014).Article 

    Google Scholar 
    Hollander, M. & Wolfe, D. A. Nonparametric statistical methods. Ergonomics 18, 701–702 (1975).
    Google Scholar 
    Kohler, K. E. & Gill, S. M. Coral point count with excel extensions (CPCe): A visual basic program for the determination of coral and substrate coverage using random point count methodology. Comput. Geosci. 32, 1259–1269. https://doi.org/10.1016/j.cageo.2005.11.009 (2006).ADS 
    Article 

    Google Scholar 
    Geller, J., Meyer, C., Parker, M. & Hawk, H. Redesign of PCR primers for mitochondrial cytochrome c oxidase subunit I for marine invertebrates and application in all-taxa biotic surveys. Mol. Ecol. Resour. 13, 851–861. https://doi.org/10.1111/1755-0998.12138 (2013).CAS 
    Article 
    PubMed 

    Google Scholar 
    Hao, X., Jiang, R. & Chen, T. Clustering 16S rRNA for OTU prediction: A method of unsupervised Bayesian clustering. Bioinformatics 27, 611–618. https://doi.org/10.1093/bioinformatics/btq725 (2011).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581. https://doi.org/10.1038/nmeth.3869 (2016).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2020).Ranwez, V., Harispe, S., Delsuc, F. & Douzery, E. J. P. MACSE: Multiple alignment of coding SEquences accounting for frameshifts and stop codons. PLoS ONE https://doi.org/10.1371/journal.pone.0022594 (2011).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Machida, R. J., Leray, M., Ho, S. L. & Knowlton, N. Data Descriptor: Metazoan mitochondrial gene sequence reference datasets for taxonomic assignment of environmental samples. Sci. Data https://doi.org/10.1038/sdata.2017.27 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261–5267. https://doi.org/10.1128/aem.00062-07 (2007).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Generate High-Resolution Venn and Euler Plots v. 1.6.20 (2018).Ginestet, C. ggplot2: Elegant graphics for data analysis. J. R. Stat. Soc. Ser. Stat. Soc. 174, 245–245. https://doi.org/10.1111/j.1467-985X.2010.00676_9.x (2011).Article 

    Google Scholar 
    McMurdie, P. J. & Holmes, S. phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE https://doi.org/10.1371/journal.pone.0061217 (2013).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Anderson, M. J. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26, 32–46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x (2001).Article 

    Google Scholar 
    Hervé, M. Testing and plotting procedures for biostatistics v. 0.9-79. Retrieved from https://cran.r-project.org/web/packages/RVAideMemoire/index.html (2021).De Caceres, M. & Legendre, P. Associations between species and groups of sites: Indices and statistical inference. Ecology 90, 3566–3574. https://doi.org/10.1890/08-1823.1 (2009).Article 
    PubMed 

    Google Scholar 
    Legendre, P. & Anderson, M. J. Distance-based redundancy analysis: Testing multispecies responses in multifactorial ecological experiments. Ecol. Monogr. 69, 1–24. https://doi.org/10.1890/0012-9615(1999)069[0001:dbratm]2.0.co;2 (1999).Article 

    Google Scholar 
    Roberts, D. Ordination and multivariate analysis for ecology v. 2.0-1. Retrieved from http://ecology.msu.montana.edu/labdsv/R (2019).Dray, S., Bauman, D., Blanchet, G., Borcard, D., Clappe, S., Guenard, G. & Wagner, H. Adespatial: Multivariate multiscale spatial analysis v. 0.3-13. Retrieved from https://cran.r-project.org/package=adespatial (2021). More

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    Spatial structure of city population growth

    Overview of U.S. domestic migration flowsThe most recent ACS county-to-county flow dataset26 reports that about 45.6 million people migrated to the U.S. per year during the period 2015–2019, which corresponds to 14.2% of the U.S. population27. Approximately 43.5 million annual moves corresponded to domestic migration (moves within the U.S.28), while 2.1 million accounted for inflows of individuals from other countries (viz. international immigration).With respect to domestic migration, 25.7 million people per year migrated within the same county, thus showing that the highest share of domestic flows (59%) is intra-county. Annually, about 10.4 people moved between different counties within the same state, thus intra-state flows account for 24% of the domestic migration (Supplementary Fig. 1), mainly driven by the search for more affordable housing, better jobs, and for family reasons such as change in marital status29. Long distance moves, captured by inter-state flows, represent the remaining 17% of domestic flows, which comprises about 7.5 million moves per year. Here, we will refer to these domestic migration flows as inflows or outflows, and netflows (inflows-outflows).The United States Office of Management and Budget (OMB) classifies counties as metropolitan, micropolitan, or neither30. A metropolitan statistical area contains a core urban area of at least 50,000 population. A metro area represents a functional delineation of an urban area with a network of strong socioeconomic ties, and provision of infrastructure services31,32,33. A micropolitan statistical area contains an urban core of at lest 10,000 but less than 50,000 inhabitants. There are over 380 metropolitan statistical areas in the U.S., each composed of one or more counties, accounting for about 86% of the total U.S. population and comprising approximately 28% of the land area of the country. For this reason, our analysis focuses on the growth dynamics of MSA counties. Supplementary Fig. 2 shows the 3141 counties (administrative subdivisions of the states) in the U.S., comprising about 321 million inhabitants in the starting year of the ACS 5-Year survey period (2015–2019) of our analysis26.Population growth has two components, namely natural growth and migration. Natural growth accounts for births minus deaths, and migration comprises domestic and international migration. With recent trends showing that births and natural increase have declined in the U.S. and in recent years contribute less to overall city population growth34,35, migration patterns become more relevant to the study of city population growth. Because the ACS flow files contain international inflows only, the relative importance of migrations on population growth is here addressed by x = ∣Inflows−Outflows∣/∣Births−Deaths∣ (Supplementary Figs. 3, 4), which is the ratio between domestic netflows and natural growth. The statistical distribution of this quantity computed for all U.S. counties is well fitted by a lognormal distribution, and shows that x≥1 for 76.5% of counties. For most counties, domestic migration dominates population growth, and understanding the spatial structure of domestic netflows (and their distribution within a city) is crucial to the comprehension of the mechanisms behind the heterogeneity of city population growth.At this spatial granularity, we observe a strong heterogeneity among the U.S. counties (Supplementary Fig. 2) for the period 2015 − 2019, along with examples of specific MSAs. In particular, the relative dispersion of counties relative growth due to netflows is higher than one for about 85% of the metro areas, indicating a large heterogeneity within the same city and pointing towards the spatial structure of domestic migration. The observed difference in the netflows stresses the relevance of our approach: counties belonging to the same city may have specific growth rates due to population flow patterns, thus indicating preferential flow destinations and pinpointing the direction in which the city has expanded.Heterogeneity of inter- and intra-city flowsInter-city flows represent the major component of the total flows (~55%), while intra-city flows represent ~25%. Flows between metro and micro areas, and between metro and non-statistical areas are the smallest components, with ~13% and ~7%, respectively. Given that about 80% of the domestic migration are composed of intra- and inter-city flows, we will focus our attention on describing the structure of intra- and inter-city flows, but in the Supplementary Information we offer a brief analysis of flows between metro and micro areas, and between metro and non-statistical areas.Inter-city flows are not uniform across the U.S. cities. The most intense annual netflows ( >2000 people per year), accounting for approximately 17% of the entire inter-city U.S. netflows, are mainly from New York and Chicago to California and Florida (Fig. 2), and from Los Angeles to neighboring cities. Notably, netflows among the Midwestern cities are mostly negative and below the threshold we set. These flows are mainly responsible for increasing or decreasing the population of a given city. Intra-city flow patterns, illustrated with the 7 most populous U.S. cities with more than 5 counties, are also non-uniform.Fig. 2: Heterogeneity of inter- and intra-city netflows.The map (A) suggests that the domestic redistribution of people between different U.S. metro areas are non-uniform: the black arrows, indicating the direction of the most intense inter-city netflows (higher than 2000 people per year), reveal migration trends from northern and eastern cities to western and southern regions. Cities (composed of one or more counties) are colored according to the relative growth (viz. population growth adjusted by population) of the whole MSA during the 2015–2019 period, and the black intensity and the thickness of the arrows are proportional to the netflows. Alaska and Hawaii are not shown. Panels (B–H), which are close-up of New York (B), Chicago (C), Dallas (D), Houston (E), Washington D.C. (F), Philadelphia (G), Atlanta (H), suggest that the most intense intra-city netflows are oriented radially outwards: people are moving from core to external counties. Here, counties are colored according to their relative growth in the 2015–2019 period and the width of the arrows is proportional to the netflows between origin and destination counties.Full size imageOur analysis reveals that city centers (defined as the core county with the highest population density) are more likely to have negative netflows, indicating that people are leaving the central regions of cities. The arrows in Fig. 2 indicate the direction of the most intense netflows, supporting this finding and highlighting that there is a trend of people moving from internal to external regions, contributing to population growth and spatial expansion of U.S. cities. In fact, we found no correlation between relative population growth (viz. population growth by county size) and distance from the core county (Supplementary Fig. 5A) for the 46 cities with more than 5 counties, with relative growth about 0.03 ± 0.05. On the other hand, we found that relative natural growth (Supplementary Fig. 5B) is negatively correlated with the distance to core county, thus natural growth is less relevant as a component of growth in the outer regions of cities. Consequently, our results show that not only the contribution of each component of growth changes with distance to core county, but also that the internal redistribution of people is an important mechanism of growth, mainly in the external counties.We also examined variability in inter- and intra-city flows within the 50 states (Supplementary Fig. 6). Total flows within a state increase, as expected, with the state population. Two special cases are, however, of interest: (1) two states (Vermont and Rhode Island) with small populations have only one MSA, in which case within-state inter-city flows are zero; and (2) nearly 40%, or 149, of MSAs have only one county, in which case intra-city flows could not be estimated. For all other cases, we observe on average an equal split between inter- and intra-city flows, but with considerable variability among the states, with a mean about 0.5 and standard deviation about 0.2. A generalization of the intra- and inter-city migratory patterns for all 46 cities with more than 5 counties shows that the percentage of migrants from intra- and inter-city flows are of the same order of magnitude (Fig. 3).Fig. 3: Roles of intra- and inter-city flows in driving the heterogeneous population growth of cities.We define the core county as the one with the highest population density, and we plot the percentage of inflows due to intra- (A) and inter-city flows (B) of each county within a city as a function of its distance to the core county. The percentage of outflows due to intra- and inter-city flows are shown in (C) and (D), respectively. The positive correlation of the relative growth with distance due to intra-city flows in (E), along with the lack of correlation due to inter-city flows in (F), indicates that intra-city flows are mainly responsible for increasing the population in the external regions of cities. The sizes of red circles and blue squares are proportional to the city population. The range of distances is split into equally spaced bins. The number of counties n within each bin, from left to right, is 46, 1, 4, 7, 7, 17, 21, 31, 36, 38, 34, 31, 31, 30, 20, 20, 21, 14, 17, 9, 9, 6, 4, 2, 5, 5, 2, 1. The black dots and the error bars indicate the mean and the 90% interval, respectively, of the counties within the corresponding bin. We also show the Pearson correlation coefficient R and the p-value associated with the two-sided test of the null hypothesis of non-correlation.Full size imageApart from the core county, flows from the same city correspond to about 50% of the inflow of people in the counties, presenting a slightly positive correlation with their distance from the city center (Fig. 3A). The low percentage for the core county indicates that it is not the major destination of flows from the same city. The percentage of inflows from other cities is higher in the core county and decays as we move towards the suburbs (Fig. 3B). The moderate negative correlation of this percentage with the distance reveals that inflows from other cities are more likely to concentrate in the core regions of a city.The percentage of outflows directed from the core county to other counties within the same city has a slightly negative correlation with the distance of the origin county to the city center, so it is more likely to find intra-city flows with outflows from internal regions (Fig. 3C). The core county is an exception again, suggesting that it is less likely that someone leaving the core county will move to another county within the same city. The slightly negative correlation of the percentage of outflows directed to other cities suggests that there is a trend of people leaving the core county and the central regions to move to other cities (Fig. 3D). The high percentage of inflows (Fig. 3B) and outflows (Fig. 3D) in the central region due to inter-city flows implies that the central regions of cities are more dynamic and diverse and that people tend to move to counties with similar levels of urbanization. The same pattern is observed for flows between metro and micro areas, and for metro and non-statistical areas, allowing us to conclude that people moving from rural areas are more likely to move to the external regions of a city (Supplementary Fig. 7).The positive correlation of the relative growth with the distance due to intra-city flows (Fig. 3E) shows that the resulting intra-city redistribution of people, given by the difference between inflows and outflows, is such that there is a trend from core county to the external counties (viz. suburbs). When compared to the relative growth due to inter-city flows (Fig. 3F), which do not show any trend and that have negative values for the most distant counties, it becomes clear that intra-city flows play a major role in the population increase observed in outer regions of cities. Interestingly, large circle and square dots in Fig. 3E and F suggest that the loss of people due to inter-city netflows is more intense than the gain of people due to intra-city netflows in some external counties of the largest metro areas, thus explaining the population decline in some outer regions of New York and Chicago (as shown in Fig. 2B and C).The population growth due to intra-city flows is also depicted in Fig. 4. The concentration of flows below the diagonal captures the heterogeneity and the preferential destination of intra-city netflows. We observe that people are more likely to move to lower population density counties when moving from one place to another within the same city, as exemplified by 7 cities in panel A. Panel B summarizes this analysis for the 46 cities with more than 5 counties by showing the fraction ({{{{{{{mathcal{F}}}}}}}}) of intra-city netflows to lower density counties. We note that more than 93% of the cities have ({{{{{{{mathcal{F}}}}}}}} > 0.5) and that there is a positive correlation of ({{{{{{{mathcal{F}}}}}}}}) with the city population, and C shows the rank of cities according to the fraction of intra-city netflows to lower density counties.Fig. 4: People are moving to counties with lower population density.A The population density of the origin (ρo) and destination (ρd) counties of intra-city netflows for New York, Chicago, Dallas, Houston, Washington D.C., Philadelphia, Atlanta, reveal that the majority of the flows occur from high to low-density counties. The size of the symbols are proportional to the intensity of the netflow, and the black line corresponds to y = x. B The fraction of netflows to lower density counties ({{{{{{{mathcal{F}}}}}}}}) has a positive correlation with city population when we consider the 46 MSAs with more than 5 counties, suggesting that intra-city netflows to lower density counties are more frequent as the city size increases. We also show the Pearson correlation coefficient R and the p-value associated with the two-sided test of the null hypothesis of non-correlation. C The ranking of the cities according to ({{{{{{{mathcal{F}}}}}}}}).Full size imagePopulation density does not seem to play a major role in driving flows between counties of different cities. The fraction of inter-city netflows to lower density counties is about 57% when we consider all the 384 MSAs. The heterogeneity in the inter-city netflow pattern can be assessed by analyzing ({{{{{{{mathcal{F}}}}}}}}) versus the population of the destination city (Fig. 5A, B) and ({{{{{{{mathcal{F}}}}}}}}) versus the population of the origin city (Fig. 5C, D). The negative correlation of ({{{{{{{mathcal{F}}}}}}}}) with the population of the destination city in panel A indicates that inflows are more likely to come from lower density counties as the destination city size increases. The positive correlation of ({{{{{{{mathcal{F}}}}}}}}) with the population of the origin city in panel C reveals that outflows tend to be directed to lower density counties as the origin city size increases. The trends observed in panels A and C reveal that inter-city flows are more likely between counties with different population densities rather than between counties with similar population densities. Panels B and D show the rank order of cities according to a function of the destination city size and the origin city size, respectively.Fig. 5: Inter-city flow patterns depend on the population size of the origin and destination cities.Each point corresponds to a particular city. A Fraction ({{{{{{{mathcal{F}}}}}}}}) of netflows going to lower density counties versus the population of the destination city. Inflows to counties of large cities (with population greater than 106, dashed line) usually comes from counties with lower population densities. B Rank of cities according to the share of inflows from lower density counties. C Fraction ({{{{{{{mathcal{F}}}}}}}}) versus the population of the origin city. Outflows from counties of large cities usually go to cities with lower density counties. D The rank of cities according to the share of inter-city netflows to lower density counties is presented. The dots are colored according to the city population density (darker red means higher density). We also show the Pearson correlation coefficient R and the p-value associated with the two-sided test of the null hypothesis of non-correlation.Full size imageWe would expect that there might be preferential locations within a given city to which people move due to various factors such as lower costs of housing and employment opportunities. However, it seems that house prices have little to no effect on intra-city netflows (Supplementary Fig. 8). While the fraction of intra-city netflows to counties with less expensive houses is about 0.8 for cities like New York, Chicago and Washington, this fraction is about 0.2 for cities like Dallas, Houston and Philadelphia. The lack of a clear national pattern highlights the specificity of each city and the heterogeneity of the regional housing market in the U.S.36,37. On the other hand, the fraction of intra-city netflows to counties with lower unemployment rates is higher than 0.5 for about 2/3 of the cities (Supplementary Fig. 9), thus showing that people are more likely to move to counties with lower unemployment rates.Statistical structure of inter-city flowsIntra-city flows capture the internal redistribution of population, without altering the total city population. In this context, we focus on inter-city flows to investigate whether or not extreme flows play an important role in shaping the growth of counties as observed at the city level5. For cities, Verbavatz and Barthelemy5 introduce a stochastic equation to describe population growth, composed of two terms. The first term accounts for out-of-system growth, which includes natural growth and international migration, and the second term accounts for the growth due to domestic netflows. They find that total netflows adjusted by population size can be well approximated by a Lévy distribution, and this heavy-tailed distribution indicates that rare and extreme inter-city flows (viz. migratory shocks) dominate city population growth.Here, we find that, for counties, the distribution of total netflows adjusted by population size, which is represented by ζi and captures the intensity of inter-city migratory flows (see the section “Methods” for details), can be approximated by a Gaussian distribution (Fig. 6). The lack of a heavy tail in the empirical distribution of ζi suggests the absence of extreme flows at the county level, thus indicating that the growth of counties can be described by smoother migratory process than cities. Given that cities do experience migratory shocks5, our findings indicate that cities redistribute inflows among its different counties, leading to a spill-over effect that dampens flow shocks at the county level.Fig. 6: Extreme shocks are dissipated at the county level.The distribution of ζi, which is the sum of the netflows of a county i adjusted by its population, suggests that migratory events are exponentially bounded at the county level since ζi is well described by a Gaussian distribution. The distribution of ζi is computed here for all the counties with at least 50.000 inhabitants. We also show the result of the two-sided KS test under the null hypothesis that ζi follows a Gaussian distribution.Full size imageHeterogeneity of international inflowsThe highest share of international inflows is concentrated in large cities. About 40% of the international inflows are destined to the top 10 (~2.6%) largest metro areas of the U.S. New York is the first with 8.5% of international inflows, followed by Los Angeles and Miami with 5.4% and 5.0%, respectively. Indeed, international inflows Yk scale superlinearly with the population Sk of the metro area k (Fig. 7A), thus larger cities have more immigrants per capita than smaller cities.Fig. 7: International inflow scales superlinearly with city size.Panel (A) shows the number of international immigrants as a function of the city size S for the 384 U.S. metro areas. The performance of the model Y = Y0Sθ, in which θ = 1.19 (95% CI [1.13, 1.24]) and Y0 = 4.10−4 is a normalization constant, is assessed by the coefficient of determination R2. Note that the spread of empirical data around the model narrows as the size of the city increases. Panel (B) shows the rank of the metro areas and the residues, which captures the deviation from the null model thus highligthing cities receiving more/less than expected international inflows. Names of the cities are followed by two-letter state abbreviations.Full size imageInterestingly, this gain with scale is also observed in socioeconomic city metrics as crime, GDP, innovation and wealth creation due to the manifestation of nonlinear agglomeration phenomena38,39,40. Using Y = Y0Sθ as a null model, we can compute deviations from the average behavior by means of residuals given by (log ({Y}_{k}/{Y}_{0}{S}_{k}^{theta }))38. The rank of the residues (Fig. 7B) shows that college towns are among the top metro areas receiving more international inflows than expected, while large cities as Los Angeles, New York, Atlanta, and Chicago are among the metro areas receiving less international inflows than expected.The spatial distribution of international inflows within cities is shown in Supplementary Fig. 10. The highest share of inflows is concentrated at core counties, and the percentage of inflows decreases dramatically with the distance from the core county. This result suggests that inflow of international migrants is an important component of population growth, particularly at the core regions of large cities.Robustness of our findingsPatterns of population redistribution change from time to time in the U.S., and are affected by several factors. For instance, in the 1960s non-metropolitan counties lost about 3 million people due to outflows to metropolitan counties, while the reverse trend was observed in the 1970s when non-metropolitan counties experienced net inflows of about 2.6 million people41. Wardwell and Brown in41 indicate that three factors might be among the main reasons of such change, namely economic decentralization, preference for rural living, and modernization of rural life. The temporal influence of factors as socioeconomic conditions, transportation infrastructure, natural amenities, and land use and development on population growth in rural and suburban areas is explored in42. Changes in rural migration patterns are also studied in43, where age-specific rural migration patterns from 1950 to 1995 are analyzed. In44, the authors explore redistribution trends across U.S. counties from 1980 to 1995 split into three five year periods (1980–1985, 1985–1990, 1990–1995), and45 analyzes changes in age-specific nationwide migration patterns from 1950 to 2010.The spatial structure of migration patterns may indeed change from time to time; our results correspond to the current intra- and inter-city redistribution trends, based on the most recent ACS migration flow files. We present a thorough empirical and statistical analysis of domestic migration flows among U.S. cities ans counties. Our study also introduces a framework that can be used for analyzing and comparing internal redistribution of people across different time periods. Indeed, we extended our analysis for two other time periods, 2005–2009 and 2010–2014. With respect to the spatial distribution of intra- and inter-city flows, similar trends are observed in both periods (Supplementary Figs. 12, 13), namely inter-city flows are responsible for the highest share of inflows to core counties, and intra-city flows are responsible for the highest share of inflows to external counties. We also explored the role of population density in driving netflows between counties within the same metro area in 2005–2009 and 2010–2014. The results (Supplementary Figs. 14 and 15) indicate that 95.7% of cities were dominated by intra-city moves to lower density counties in 2005–2009, and this percentage dropped to 76.1% in 2010–2014. Our findings indicate that the trends we report here are taking place since 2005 but with different intensities.The robustness of our findings is checked with additional migration data from the Internal Revenue Service (IRS), which reports the year-to-year address changes on individual tax returns filled with the IRS46. The results obtained with the analysis of IRS datasets from periods 2015–2016, 2016–2017, 2017–2018, 2018–2019 (Supplementary Figs. 16, 17, 18, 19), reveal similar trends to those we found using ACS data. Particularly, we observe that, for all periods considered, the correlation between intra-city netflow/S and distance to core county is stronger than we found with ACS data, thus highlighting the role of intra-city flows in driving population to external regions of cities. The main difference between both datasets is in the percentage of intra- and inter-city inflows and outflows: while ACS data indicates that both flows have approximately the same contribution to the total flows, the IRS data indicates that, besides the core county, intra-city flows are responsible for about 80% of inflows and outflows of metro areas. More

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    Ornaments are equally informative in male and female birds

    Amundsen, T. In Animal Signals: Signalling and Signal Design in Animal Communication (eds. Espmark, Y., Amundsen, T. & Rosenqvist, G.) 133–154 (Tapir Academic Press, 2000).Amundsen, T. Why are female birds ornamented? Trends Ecol. Evol. 15, 149–155 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    Lande, R. Sexual dimorphism, sexual selection and adaptation in polygenic characters. Evolution 34, 292–305 (1980).PubMed 
    Article 

    Google Scholar 
    Poissant, J., Wilson, A. J. & Coltman, D. W. Sex-specific genetic variance and the evolution of sexual size dimorphism: a systematic review of cross-sex genetic correlations. Evolution 64, 97–107 (2009).PubMed 
    Article 

    Google Scholar 
    Nordeide, J. T., Kekäläinen, J., Janhunen, M. & Kortet, R. Female ornaments revisited—are they correlated with offspring quality? J. Anim. Ecol. 82, 26–38 (2013).PubMed 
    Article 

    Google Scholar 
    Prum, R. O. The Evolution of Beauty: How Darwin’s Forgotten Theory of Mate Choice Shapes the Animal World and Us (Doubleday, 2017).Clark, C. J. & Rankin, D. Subtle, pervasive genetic correlation between the sexes in the evolution of dimorphic hummingbird tail ornaments. Evolution 74, 528–543 (2020).PubMed 
    Article 

    Google Scholar 
    LeBas, N. R. Female finery is not for males. Trends Ecol. Evol. 21, 170–173 (2006).PubMed 
    Article 

    Google Scholar 
    Kraaijeveld, K., Kraaijeveld-Smit, F. J. L. & Komdeur, J. The evolution of mutual ornamentation. Anim. Behav. 74, 657–677 (2007).Article 

    Google Scholar 
    Tobias, J. A., Montgomerie, R. & Lyon, B. E. The evolution of female ornaments and weaponry: social selection, sexual selection and ecological competition. Philos. Trans. R. Soc. B 367, 2274–2293 (2012).Article 

    Google Scholar 
    Hare, R. M. & Simmons, L. W. Sexual selection and its evolutionary consequences in female animals. Biol. Rev. 94, 1464–7931 (2019).Article 

    Google Scholar 
    Hernández, A., Martínez-Gómez, M., Beamonte-Barrientos, R. & Montoya, B. Colourful traits in female birds relate to individual condition, reproductive performance and male-mate preferences: a meta-analytic approach. Biol. Lett. 17, 20210283 (2021).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Tsuboi, M., Gonzalez-Voyer, A., Höglund, J. & Kolm, N. Ecology and mating competition influence sexual dimorphism in Tanganyikan cichlids. Evol. Ecol. 26, 171–185 (2012).Article 

    Google Scholar 
    Andersson, M. Sexual Selection (Princeton Univ. Press, 1994).Doutrelant, C., Fargevieille, A. & Grégoire, A. Evolution of female coloration: what have we learned from birds in general and blue tits in particular. Adv. Study Behav. 52, 123–202 (2020).Article 

    Google Scholar 
    Dunn, P. O., Armenta, J. K. & Whittingham, L. A. Natural and sexual selection act on different axes of variation in avian plumage color. Sci. Adv. 1, e1400155 (2015).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Cotton, S., Fowler, K. & Pomiankowski, A. Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis? Proc. Biol. Sci. 271, 771–783 (2004).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bonduriansky, R. & Rowe, L. Sexual selection, genetic architecture, and the condition dependence of body shape in the sexually dimorphic fly Prochyliza xanthostoma (Piophilidae). Evolution 59, 138–151 (2005).PubMed 
    Article 

    Google Scholar 
    Johnstone, R. A., Rands, S. A. & Evans, M. R. Sexual selection and condition-dependence. J. Evol. Biol. 22, 2387–2394 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    Cotton, S., Fowler, K. & Pomiankowski, A. Heightened condition dependence is not a general feature of male eyespan in stalk-eyed flies (Diptera: Diopsidae). J. Evol. Biol. 17, 1310–1316 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    David, P. et al. Male sexual ornament size but not asymmetry reflects condition in stalk-eyed flies. Proc. R. Soc. Lond. B 265, 2211–2216 (1998).Article 

    Google Scholar 
    Bolund, E., Schielzeth, H. & Forstmeier, W. No heightened condition dependence of zebra finch ornaments—a quantitative genetic approach. J. Evol. Biol. 23, 586–597 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    Zahavi, A. Mate selection-a selection for a handicap. J. Theor. Biol. 53, 205–214 (1975).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Meunier, J., Figueiredo Pinto, S., Burri, R. & Roulin, A. Eumelanin-based coloration and fitness parameters in birds: a meta-analysis. Behav. Ecol. Sociobiol. 65, 559–567 (2011).Article 

    Google Scholar 
    Weaver, R. J., Santos, E. S. A., Tucker, A. M., Wilson, A. E. & Hill, G. E. Carotenoid metabolism strengthens the link between feather coloration and individual quality. Nat. Commun. 9, 73 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    White, T. E. Structural colours reflect individual quality: a meta-analysis. Biol. Lett. 16, 20200001 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Cohen, J. Statistical Power Analysis for the Behavioral Sciences (Taylor & Francis Inc., 1988)Andersson, M. Sexual selection, natural selection and quality advertisement. Biol. J. Linn. Soc. 17, 375–393 (1982).Article 

    Google Scholar 
    Walther, B. A. & Clayton, D. H. Elaborate ornaments are costly to maintain: evidence for high maintenance handicaps. Behav. Ecol. 16, 89–95 (2005).Article 

    Google Scholar 
    Folstad, I. & Karter, A. K. Parasites, bright males and the immunocompetence handicap. Am. Nat. 139, 603–622 (1992).Article 

    Google Scholar 
    Alonso-Alvarez, C., Bertrand, S., Faivre, B., Chastel, O. & Sorci, G. Testosterone and oxidative stress: the oxidation handicap hypothesis. Proc. R. Soc. Lond. B 274, 819–825 (2007).CAS 

    Google Scholar 
    Weaver, R. J., Koch, R. E. & Hill, G. E. What maintains signal honesty in animal colour displays used in mate choice? Philos. Trans. R. Soc. B 372, 20160343 (2017).Article 

    Google Scholar 
    Emlen, D. J., Warren, I. A., Johns, A., Dworkin, I. & Lavine, L. C. A mechanism of extreme growth and reliable signaling in sexually selected ornaments and weapons. Science 337, 860–864 (2012).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Huhta, E. Plumage brightness of prey increases predation risk: an among-species comparison. Ecology 84, 1793–1799 (2003).Article 

    Google Scholar 
    Tibbetts, E. A. & Dale, J. A socially enforced signal of quality in a paper wasp. Nature 432, 18–222 (2004).Article 

    Google Scholar 
    Webster, M. S., Ligon, R. A. & Leighton, G. M. Social costs are an underappreciated force for honest signalling in animal aggregations. Anim. Behav. 143, 167–176 (2018).Article 

    Google Scholar 
    Sheldon, B. C. Differential allocation: tests, mechanisms and implications. Trends Ecol. Evol. 15, 397–402 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    Johnstone, R. A., Reynolds, J. D. & Deutsch, J. C. Mutual mate choice and sex differences in choosiness. Evolution 50, 1382–1391 (1996).PubMed 
    Article 

    Google Scholar 
    Promislow, D. E. L., Montgomerie, R. & Martin, T. E. Mortality costs of sexual dimorphism in birds. Proc. R. Soc. Lond. B 250, 143–150 (1992).ADS 
    Article 

    Google Scholar 
    Guindre-Parker, S. & Love, O. P. Revisiting the condition-dependence of melanin-based plumage. J. Avian Biol. 45, 29–33 (2014).Article 

    Google Scholar 
    Roulin, A. & Dijkstra, C. Genetic and environmental components of variation in eumelanin and phaeomelanin sex-traits in the barn owl. Heredity 90, 359–364 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    Jawor, J. M. & Breitwisch, R. Melanin ornaments, honesty, and sexual selection. Auk 120, 249–265 (2003).Article 

    Google Scholar 
    Gunderson, A. R., Frame, A. M., Swaddle, J. P. & Forsyth, M. H. Resistance of melanized feathers to bacterial degradation: is it really so black and white? J. Avian Biol. 39, 539–545 (2008).Article 

    Google Scholar 
    Ruiz-de-Castañeda, R., Burtt, E. H. Jr., González-Braojos, S. & Moreno, J. Bacterial degradability of an intrafeather unmelanized ornament: a role for feather-degrading bacteria in sexual selection? Biol. J. Linn. Soc. 105, 409–419 (2012).Article 

    Google Scholar 
    Tazzyman, S. J., Iwasa, Y. & Pomiankowski, A. Signaling efficacy drives the evolution of larger sexual ornaments by sexual selection. Evolution 68, 216–229 (2014).PubMed 
    Article 

    Google Scholar 
    Dale, J., Dey, C. J., Delhey, K., Kempenaers, B. & Valcu, M. The effects of life history and sexual selection on male and female plumage colouration. Nature 527, 367–370 (2015).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Guilford, T. & Dawkins, M. S. Receiver psychology and the evolution of animal signals. Anim. Behav. 42, 1–14 (1991).Article 

    Google Scholar 
    Tazzyman, S. J., Iwasa, Y. & Pomiankowski, A. The handicap process favors exaggerated, rather than reduced, sexual ornaments. Evolution 68, 2534–2549 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Peters, J. L. et al. Assessing publication bias in meta-analyses in the presence of between-study heterogeneity. J. R. Stat. Soc. Ser. A. 173, 575–591 (2010).MathSciNet 
    Article 

    Google Scholar 
    Dumbacher, J. P. & Fleischer, R. C. Phylogenetic evidence for colour pattern convergence in toxic pitohuis: Müllerian mimicry in birds? Proc. Biol. Sci. 268, 1971–1976 (2001).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Jønsson, K. A., Delhey, K., Sangster, G., Ericson, P. G. P. & Irestedt, M. The evolution of mimicry of friarbirds by orioles (Aves: Passeriformes) in Australo-Pacific archipelagos. Proc. R. Soc. B Biol. Sci. B 283, 20160409 (2016).Article 

    Google Scholar 
    Ord, T. J. & Stuart-Fox, D. Ornament evolution in dragon lizards: multiple gains and widespread losses reveal a complex history of evolutionary change. J. Evol. Biol. 19, 797–808 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G. & PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 6, e1000097 (2009).O’Dea, R. E. et al. Preferred reporting items for systematic reviews and meta-analyses in ecology and evolutionary biology: a PRISMA extension. Biol. Rev. 96, 1695–1722 (2021).PubMed 
    Article 

    Google Scholar 
    LeBas, N. R., Hockham, L. R. & Ritchie, M. G. Nonlinear and correlational sexual selection on ‘honest’ female ornamentation. Proc. R. Soc. Lond. B 270, 2159–2165 (2003).Article 

    Google Scholar 
    Ouzzani, M., Hammady, H., Fedorowicz, Z. & Elmagarmid, A. Rayyan—a web and mobile app for systematic reviews. Syst. Rev. 5, 210 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rohatgi, A. WebPlotDigitizer. Software version 4.5. https://automeris.io/WebPlotDigitizer (2000).Sidney, S. Nonparametric Statistics for the Behavioral Sciences (McGraw-Hill,1956).Friedman, H. Simplified determination of statistical power, magnitude of effect and research sample sizes. Educ. Psychol. Meas. 42, 521–526 (1982).Article 

    Google Scholar 
    Nakagawa, S. & Cuthill, I. C. Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol. Rev. 82, 591–605 (2007).PubMed 
    Article 

    Google Scholar 
    Verhulst, S. & Nilsson, J. A. The timing of birds’ breeding seasons: a review of experiments that manipulated timing of breeding. Philos. Trans. R. Soc. Lond. B 363, 399–410 (2008).Article 

    Google Scholar 
    Brown, M. E. In Current Ornithology (eds. Nolan, V. & Ketterson, E. D.) 67–135 (Plenum Press, 1996).Labocha, M. K. & Hayes, J. P. Morphometric indices of body condition in birds: a review. J. Ornithol. 153, 1–22 (2012).Article 

    Google Scholar 
    Sánchez, C. A. et al. On the relationship between body condition and parasite infection in wildlife: a review and meta-analysis. Ecol. Lett. 20, 1869–1884 (2018).Article 

    Google Scholar 
    Arnholt, A. T. & Evans, B. BSDA: Basic statistics and data analysis. R package version 1.2.0. https://cran.r-project.org/package=BSDA (2017).Jackson, D., White, I. R., Price, M., Copas, J. & Riley, R. D. Borrowing of strength and study weights in multivariate and network meta-analysis. Stat. Methods Med. Res. 26, 2853–2868 (2017).MathSciNet 
    PubMed 
    Article 

    Google Scholar 
    Hadfield, J. D. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R Package. J. Stat. Softw. 33, 1–22 (2010).Article 

    Google Scholar 
    Jetz, W., Thomas, G. H., Joy, J. B., Hartmann, K. & Mooers, A. O. The global diversity of birds in space and time. Nature 491, 444–448 (2012).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Nakagawa, S. & De Villemereuil, P. A general method for simultaneously accounting for phylogenetic and species sampling uncertainty via Rubin’s rules in comparative analysis. Syst. Biol. 68, 632–641 (2019).PubMed 
    Article 

    Google Scholar 
    Cinar, O., Nakagawa, S. & Viechtbauer, W. Phylogenetic multilevel meta-analysis: a simulation study on the importance of modeling the phylogeny. Methods Ecol. Evol. 13, 383–395 (2022).Article 

    Google Scholar 
    Viechtbauer, W. Conducting meta-analyses in R with the metafor package. J. Stat. Softw. 36, 1–48 (2010).Article 

    Google Scholar 
    Egger, M., Davey Smith, G., Schneider, M. & Minder, C. Bias in meta-analysis detected by a simple, graphical test. BMJ 315, 629–634 (1997).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Duval, S. & Tweedie, R. Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 56, 455–463 (2000).CAS 
    PubMed 
    MATH 
    Article 

    Google Scholar 
    Nakagawa, S. et al. Methods for testing publication bias in ecological and evolutionary meta-analyses. Methods Ecol. Evol. 13, 4–21 (2022).Article 

    Google Scholar 
    Nakagawa, S. & Santos, E. S. A. Methodological issues and advances in biological meta-analysis. Evol. Ecol. 26, 1253–1274 (2012).Article 

    Google Scholar 
    Billerman, S. M., Keeney, B. K., Rodewald, P. G. & Schulenberg, T. S. Birds of the World (Cornell Laboratory of Ornithology, 2000). More

  • in

    Experimental considerations of acute heat stress assays to quantify coral thermal tolerance

    Pörtner, H. O. et al. IPCC Special Report on the Ocean and Cryosphere in a Changing Cimate (2019).Genevier, L. G. C., Jamil, T., Raitsos, D. E., Krokos, G. & Hoteit, I. Marine heatwaves reveal coral reef zones susceptible to bleaching in the Red Sea. Glob. Chang. Biol. 25, 2338–2351 (2019).ADS 
    PubMed 
    Article 

    Google Scholar 
    Hughes, T. P. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science (80-.) 359, 80–83 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    Morris, L. A., Voolstra, C. R., Quigley, K. M., Bourne, D. G. & Bay, L. K. Nutrient availability and metabolism affect the stability of coral–symbiodiniaceae symbioses. Trends Microbiol. 27, 678–689 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Suggett, D. J. & Smith, D. J. Coral bleaching patterns are the outcome of complex biological and environmental networking. Glob. Chang. Biol. 26, 68–79 (2020).ADS 
    PubMed 
    Article 

    Google Scholar 
    Baker, A. C., Glynn, P. W. & Riegl, B. Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook. Estuar. Coast. Shelf Sci. 80, 435–471 (2008).ADS 
    Article 

    Google Scholar 
    Brown, B. E., Dunne, R. P., Scoffin, T. P. & Le Tissier, M. D. A. Solar damage in intertidal corals. Mar. Ecol. Prog. Ser. 105, 219–230 (1994).ADS 
    Article 

    Google Scholar 
    Suggett, D. J. & Smith, D. J. Interpreting the sign of coral bleaching as friend vs. foe. Glob. Chang. Biol. 17, 45–55 (2011).ADS 
    Article 

    Google Scholar 
    Maynard, J. A., Anthony, K. R. N., Marshall, P. A. & Masiri, I. Major bleaching events can lead to increased thermal tolerance in corals. Mar. Biol. 155, 173–182 (2008).Article 

    Google Scholar 
    Weis, V. M. The susceptibility and resilience of corals to thermal stress: adaptation, acclimatization or both?: NEWS and VIEWS. Mol. Ecol. 19, 1515–1517 (2010).PubMed 
    Article 

    Google Scholar 
    Meyer, E., Aglyamova, G. V. & Matz, M. V. Profiling gene expression responses of coral larvae (Acropora millepora) to elevated temperature and settlement inducers using a novel RNA-Seq procedure. Mol. Ecol. 20, 3599–3616 (2011).CAS 
    PubMed 

    Google Scholar 
    Dixon, G. B. et al. Genomic determinants of coral heat tolerance across latitudes. Science (80-.) 348, 1460–1462 (2015).ADS 
    CAS 
    Article 

    Google Scholar 
    Grottoli, A. G. et al. Increasing comparability among coral bleaching experiments. Ecol. Appl. 31, 1–17 (2021).Article 

    Google Scholar 
    Evensen, N. et al. Empirically derived thermal thresholds of four coral species along the Red Sea using a portable and standardized experimental approach. Coral Reefs 41, 239–252 (2022).Article 

    Google Scholar 
    Song, M. et al. The impact of acute thermal stress on the metabolome of the black rockfish (Sebastes schlegelii). PLoS ONE 14, 1–23 (2019).Article 

    Google Scholar 
    Kim, K. S. et al. Physiological responses to short-term thermal stress in mayfly (Neocloeon triangulifer) larvae in relation to upper thermal limits. J. Exp. Biol. 220, 2598–2605 (2017).PubMed 
    Article 

    Google Scholar 
    Juárez, O. E. et al. Transcriptomic and metabolic response to chronic and acute thermal exposure of juvenile geoduck clams Panopea globosa. Mar. Genomics 42, 1–13 (2018).PubMed 
    Article 

    Google Scholar 
    Pallarés, S., Arribas, P., Céspedes, V., Millán, A. & Velasco, J. Lethal and sublethal behavioural responses of saline water beetles to acute heat and osmotic stress. Ecol. Entomol. 37, 508–520 (2012).Article 

    Google Scholar 
    Qin, G. et al. Temperature-induced physiological stress and reproductive characteristics of the migratory seahorse Hippocampus erectus during a thermal stress simulation. Biol. Open 7, 1–7 (2018).CAS 

    Google Scholar 
    Zanuzzo, F. S., Bailey, J. A., Garber, A. F. & Gamperl, A. K. Comparative Biochemistry and Physiology, Part A The acute and incremental thermal tolerance of Atlantic cod (Gadus morhua) families under normoxia and mild hypoxia ☆. Comp. Biochem. Physiol. Part A 233, 30–38 (2019).CAS 
    Article 

    Google Scholar 
    Cunning, R. et al. Census of heat tolerance among Florida ’ s threatened staghorn corals finds resilient individuals throughout existing nursery populations. (2021).Evensen, N. R., Fine, M., Perna, G., Voolstra, C. R. & Barshis, D. J. Remarkably high and consistent tolerance of a Red Sea coral to acute and chronic thermal stress exposures. Limnol. Oceanogr. https://doi.org/10.1002/lno.11715 (2021).Article 

    Google Scholar 
    Morikawa, M. K. & Palumbi, S. R. Using naturally occurring climate resilient corals to construct bleaching-resistant nurseries. Proc. Natl. Acad. Sci. U. S. A. 116, 10586–10591 (2019).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rose, N. H., Bay, R. A., Morikawa, M. K. & Palumbi, S. R. Polygenic evolution drives species divergence and climate adaptation in corals. Evolution (N. Y.) 72, 82–94 (2018).
    Google Scholar 
    Thomas, L. et al. Mechanisms of thermal tolerance in reef-building corals across a fine-grained environmental mosaic: lessons from Ofu, American Samoa. Front. Mar. Sci. 4, 1–14 (2018).CAS 
    Article 

    Google Scholar 
    Voolstra, C. R. et al. Standardized short-term acute heat stress assays resolve historical differences in coral thermotolerance across microhabitat reef sites. Glob. Chang. Biol. 26, 4328–4343 (2020).ADS 
    PubMed 
    Article 

    Google Scholar 
    Klepac, C. N. & Barshis, D. J. High-resolution in situ thermal metrics coupled with acute heat stress experiments reveal differential coral bleaching susceptibility. Coral Reefs https://doi.org/10.1007/s00338-022-02276-1 (2022).Article 

    Google Scholar 
    Gardner, S. G. et al. A multi-trait systems approach reveals a response cascade to bleaching in corals. BMC Biol. 15, 117 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Madin, J. S. et al. A trait-based approach to advance coral reef science. Trends Ecol. Evol. 31, 419–428 (2016).PubMed 
    Article 

    Google Scholar 
    Suggett, D. J. et al. Toward bio-optical phenotyping of reef-forming corals using light-induced fluorescence transient-fast repetition rate fluorometry. Limnol. Oceanogr. Methods https://doi.org/10.1002/lom3.10479 (2022).Article 

    Google Scholar 
    Krueger, T. et al. Differential coral bleaching-contrasting the activity and response of enzymatic antioxidants in symbiotic partners under thermal stress. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 190, 15–25 (2015).CAS 
    Article 

    Google Scholar 
    Leggat, W. et al. Differential responses of the coral host and their algal symbiont to thermal stress. PLoS ONE 6, e26687 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Nitschke, M. R. et al. Utility of photochemical traits as diagnostics of thermal tolerance amongst great barrier reef corals. Front. Mar. Sci. 5, 1–18 (2018).Article 

    Google Scholar 
    Warner, M. E., Fittt, W. K. & Schmidt, G. W. Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc. Natl. Acad. Sci. 96, 8007–8012 (1999).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Fitt, W. K., Brown, B. E., Warner, M. E. & Dunne, R. P. Coral bleaching: Interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20, 51–65 (2001).Article 

    Google Scholar 
    Tolosa, I., Treignier, C., Grover, R. & Ferrier-Pagès, C. Impact of feeding and short-term temperature stress on the content and isotopic signature of fatty acids, sterols, and alcohols in the scleractinian coral Turbinaria reniformis. Coral Reefs 30, 763–774 (2011).ADS 
    Article 

    Google Scholar 
    Grottoli, A. G. et al. Coral physiology and microbiome dynamics under combined warming and ocean acidification. PLoS ONE 13, e0191156 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Chow, M. H., Tsang, R. H. L., Lam, E. K. Y. & Ang, P. Quantifying the degree of coral bleaching using digital photographic technique. J. Exp. Mar. Bio. Ecol. 479, 60–68 (2016).Article 

    Google Scholar 
    Nielsen, J. J. V. et al. Physiological effects of heat and cold exposure in the common reef coral Acropora millepora. Coral Reefs 39, 259–269 (2020).Article 

    Google Scholar 
    McLachlan, R. H., Price, J. T., Solomon, S. L. & Grottoli, A. G. Thirty years of coral heat-stress experiments: a review of methods. Coral Reefs 39, 885–902 (2020).Article 

    Google Scholar 
    Edmunds, P. J. & Burgess, S. C. Correction: Size-dependent physiological responses of the branching coral Pocillopora verrucosa to elevated temperature and PCO2 (J. Exp. Biol. (2016) 219 (3896-3906) doi: 10.1242/jeb.146381). J. Exp. Biol. 221, 3896–3906 (2018).Article 

    Google Scholar 
    Madin, J. S., Baird, A. H., Dornelas, M. & Connolly, S. R. Mechanical vulnerability explains size-dependent mortality of reef corals. Ecol. Lett. 17, 1008–1015 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Pausch, R. E., Williams, D. E. & Miller, M. W. Impacts of fragment genotype, habitat, and size on outplanted elkhorn coral success under thermal stress. Mar. Ecol. Prog. Ser. 592, 109–117 (2018).ADS 
    Article 

    Google Scholar 
    Shenkar, N., Fine, M. & Loya, Y. Size matters: bleaching dynamics of the coral Oculina patagonica. Mar. Ecol. Prog. Ser. 294, 181–188 (2005).ADS 
    Article 

    Google Scholar 
    Middlebrook, R., Anthony, K. R. N., Hoegh-Guldberg, O. & Dove, S. Heating rate and symbiont productivity are key factors determining thermal stress in the reef-building coral Acropora formosa. J. Exp. Biol. 213, 1026–1034 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hoey, A. et al. Recent advances in understanding the effects of climate change on coral reefs. Diversity 8, 12 (2016).Article 

    Google Scholar 
    Marhoefer, S. R. et al. Signatures of adaptation and acclimatization to reef flat and slope habitats in the coral pocillopora damicornis. Front. Mar. Sci. https://doi.org/10.3389/fmars.2021.704709 (2021).Article 

    Google Scholar 
    Cornwell, B. et al. Widespread variation in heat tolerance and symbiont load are associated with growth tradeoffs in the coral acropora hyacinthus in palau. Elife 10, 1–15 (2021).Article 

    Google Scholar 
    McClanahan, T. R. et al. Large geographic variability in the resistance of corals to thermal stress. Glob. Ecol. Biogeogr. 29, 2229–2247 (2020).Article 

    Google Scholar 
    Magozzi, S. & Calosi, P. Integrating metabolic performance, thermal tolerance, and plasticity enables for more accurate predictions on species vulnerability to acute and chronic effects of global warming. Glob. Chang. Biol. 21, 181–194 (2015).ADS 
    PubMed 
    Article 

    Google Scholar 
    Drury, C., Manzello, D. & Lirman, D. Genotype and local environment dynamically influence growth, disturbance response and survivorship in the threatened coral, Acropora cervicornis. PLoS ONE 12, 1–21 (2017).Article 

    Google Scholar 
    McLachlan, R. H., Dobson, K. L., Schmeltzer, E. R., Thurber, R. V. & Grottoli, A. G. A review of coral bleaching specimen collection, preservation, and laboratory processing methods. PeerJ 9, 1–21 (2021).Article 

    Google Scholar 
    Okubo, N., Motokawa, T. & Omori, M. When fragmented coral spawn? Effect of size and timing on survivorship and fecundity of fragmentation in Acropora formosa. Mar. Biol. 151, 353–363 (2007).Article 

    Google Scholar 
    Bruno, J. F. Fragmentation in Madracis mirabilis (Duchassaing and Michelotti): How common is size-specific fragment survivorship in corals?. J. Exp. Mar. Bio. Ecol. 230, 169–181 (1998).Article 

    Google Scholar 
    Suggett, D. J. et al. Optimizing return-on-effort for coral nursery and outplanting practices to aid restoration of the Great Barrier Reef. Restor. Ecol. 27, 683–693 (2019).Article 

    Google Scholar 
    Howlett, L., Camp, E. F., Edmondson, J., Henderson, N. & Suggett, D. J. Coral growth, survivorship and return-on-effort within nurseries at high-value sites on the Great Barrier Reef. PLoS ONE 16, 1–15 (2021).Article 

    Google Scholar 
    Veal, C. J., Carmi, M., Fine, M. & Hoegh-Guldberg, O. Increasing the accuracy of surface area estimation using single wax dipping of coral fragments. Coral Reefs 29, 893–897 (2010).ADS 
    Article 

    Google Scholar 
    Voolstra, C. R. et al. Contrasting heat stress response patterns of coral holobionts across the Red Sea suggest distinct mechanisms of thermal tolerance. Mol. Ecol. 30, 4466–4480 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Dove, S. et al. Response of holosymbiont pigments from the scleractinian coral Montipora monasteriata to short-term heat stress. Limnol. Oceanogr. 51, 1149–1158 (2006).ADS 
    Article 

    Google Scholar 
    Traylor-Knowles, N., Rose, N. H., Sheets, E. A. & Palumb, S. Early tracriptional responses during heat stress in the coral Acropora hyacinthus. Biol. Bull. 232, 91–100 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Schuback, N. et al. Single-turnover variable chlorophyll fluorescence as a tool for assessing phytoplankton photosynthesis and primary productivity: opportunities, caveats and recommendations. Front. Mar. Sci. https://doi.org/10.3389/fmars.2021.690607 (2021).Article 

    Google Scholar 
    Macadam, A., Nowell, C. J. & Quigley, K. Machine learning for the fast and accurate assessment of fitness in coral early life history. Remote Sens. 13, 1–17 (2021).Article 

    Google Scholar 
    Teague, J., Willans, J., Allen, M. J., Scott, T. B. & Day, J. C. C. Applied marine hyperspectral imaging; coral bleaching from a spectral viewpoint. Spectrosc. Eur. 31, 13–17 (2019).CAS 

    Google Scholar 
    Davies, S. W., Ries, J. B., Marchetti, A. & Castillo, K. D. Symbiodinium functional diversity in the Coral Siderastrea siderea Is influenced by thermal stress and reef environment, but not ocean acidification. Front. Mar. Sci. 5, 1–14 (2018).Article 

    Google Scholar 
    Tang, J. et al. Increased ammonium assimilation activity in the scleractinian coral pocillopora damicornis but not its symbiont after acute heat stress. Front. Mar. Sci. 7, 1–10 (2020).ADS 
    Article 

    Google Scholar 
    Sweet, M. et al. Species-specific variations in the metabolomic profiles of Acropora hyacinthus and Acropora millepora mask acute temperature stress effects in adult coral colonies. Front. Mar. Sci. 8, 1–15 (2021).Article 

    Google Scholar 
    Newton, J. R., Smith-Keune, C. & Jerry, D. R. Thermal tolerance varies in tropical and sub-tropical populations of barramundi (Lates calcarifer) consistent with local adaptation. Aquaculture 308, S128–S132 (2010).Article 

    Google Scholar 
    Waltham, N. J. & Sheaves, M. Acute thermal tolerance of tropical estuarine fish occupying a man-made tidal lake, and increased exposure risk with climate change. Estuar. Coast. Shelf Sci. 196, 173–181 (2017).ADS 
    Article 

    Google Scholar 
    Iwabuchi, B. L. & Gosselin, L. A. Implications of acute temperature and salinity tolerance thresholds for the persistence of intertidal invertebrate populations experiencing climate change. Ecol. Evol. 10, 7739–7754 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Cox, J., Schubert, A. M., Travisano, M. & Putonti, C. Adaptive evolution and inherent tolerance to extreme thermal environments. BMC Evol. Biol. https://doi.org/10.1186/1471-2148-10-75 (2010).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Quigley, K. M., Bay, L. K. & Willis, B. L. Temperature and water quality-related patterns in sediment-associated Symbiodinium communities impact symbiont uptake and fitness of juveniles in the genus Acropora. Front. Mar. Sci. 4, 1–17 (2017).Article 

    Google Scholar 
    Voolstra, C. R. et al. Extending the natural adaptive capacity of coral holobionts. Nat. Rev. Earth Environ. https://doi.org/10.1038/s43017-021-00214-3 (2021).Article 

    Google Scholar 
    Cocciardi, J. M. et al. Adjustable temperature array for characterizing ecological and evolutionary effects on thermal physiology. Methods Ecol. Evol. 2019, 1339–1346 (2019).Article 

    Google Scholar 
    Smith, G. & Spillman, C. New high-resolution sea surface temperature forecasts for coral reef management on the Great Barrier Reef. Coral Reefs 38, 1039–1056 (2019).ADS 
    Article 

    Google Scholar 
    Bainbridge, S. J. Temperature and light patterns at four reefs along the Great Barrier Reef during the 2015–2016 austral summer: understanding patterns of observed coral bleaching. J. Oper. Oceanogr. 10, 16–29 (2017).
    Google Scholar 
    Siebeck, U. E., Marshall, N. J., Klüter, A. & Hoegh-Guldberg, O. Monitoring coral bleaching using a colour reference card. Coral Reefs 25, 453–460 (2006).ADS 
    Article 

    Google Scholar 
    Palumbi, S. R., Barshis, D. J., Traylor-Knowles, N. & Bay, R. A. Mechanisms of reef coral resistance to future climate change. Science (80-.) 344, 895–899 (2014).ADS 
    CAS 
    Article 

    Google Scholar 
    Saxby, T., Dennison, W. C. & Hoegh-Guldberg, O. Photosynthetic responses of the coral Montipora digitata to cold temperature stress. Mar. Ecol. Prog. Ser. 248, 85–97 (2003).ADS 
    Article 

    Google Scholar 
    Deschaseaux, E. S. M., Deseo, M. A., Shepherd, K. M., Jones, G. B. & Harrison, P. L. Air blasting as the optimal approach for the extraction of antioxidants in coral tissue. J. Exp. Mar. Bio. Ecol. 448, 146–148 (2013).CAS 
    Article 

    Google Scholar 
    Holmes, G., Ortiz, J., Kaniewska, P. & Johnstone, R. Using three-dimensional surface area to compare the growth of two Pocilloporid coral species. Mar. Biol. 155, 421–427 (2008).Article 

    Google Scholar 
    Naumann, M. S., Niggl, W., Laforsch, C., Glaser, C. & Wild, C. Coral surface area quantification-evaluation of established techniques by comparison with computer tomography. Coral Reefs 28, 109–117 (2009).ADS 
    Article 

    Google Scholar 
    Ritchie, R. J. Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosynth. Res. 89, 27–41 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    Licthenthaler, H. K. Chlorophylls and carotenoids – pigments of photosynthetic biomembranes. Methods Enzymol. 148, 350–382 (1987).Article 

    Google Scholar 
    R Core Team. R: a language and environment for statistical computing. (2020).Hartig, F. & Lohse, L. Package ‘DHARMa’ residual diangonstics for hierarchical (multi-level/mixed) regression models (2021).Brooks, M. E. et al. glmmTMB balances speed and flexibility among packaages for zero-inflated generalized linear mixed modelling. R Journal 9, 378–400 (2017).Article 

    Google Scholar 
    Harrison, X. A. et al. A brief introduction to mixed effects modelling and multi-model inference in ecology. PeerJ 2018, 1–32 (2018).
    Google Scholar 
    Nakagawa, S. & Schielzeth, H. A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol. Evol. 4, 133–142 (2013).Article 

    Google Scholar 
    Oksanen, J. et al. Vegan (2020).Sarkar, D. Lattice: Multivariate Data Visualization with R (Springer, 2008).MATH 
    Book 

    Google Scholar  More

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    A real-time rural domestic garbage detection algorithm with an improved YOLOv5s network model

    Attention combination mechanismDue to the difficulty in extracting features from target areas in images, the high computational effort of the model and the low accuracy of detection are addressed. As shown in Fig. 3, we introduce a lightweight feedforward convolutional attention module CBAM after the backbone network Focus module of the YOLOv5s network model. The SE-Net (Squeeze and Excitation Networks) channel attention module is posted at the end of the backbone network. We propose an attention combination mechanism based on the YOLOv5s network model and name the improved network model YOLOv5s-CS. Where the CBAM module has a channel number of 128, a convolutional kernel size of 3 and a step size of 2, the SELayer has a channel number of 1024 and a step size of 4.Figure 3YOLOv5 backbone network structure before and after improvement.Full size imageConvolutional block attention module networkIn 2018, Woo et al.25 proposed the lightweight feedforward convolutional attention module CBAM. The CBAM module focuses on feature information from both channels and space dimensions and combines feature information to some extent to obtain more comprehensive reliable attentional information26. CBAM consists of two submodules, the channel attention module (CAM) and spatial attention module (SAM), and its overall module structure is shown in Fig. 4a.Figure 4Principle of CBAM.Full size imageThe working principle of the CAM is shown in Fig. 4b. First, the feature map F is input at the input entrance. Second, the global maximum pooling operation and the global average pooling operation are applied to the width and height of the feature map respectively to obtain two feature maps of the same size. Third, two feature maps of the same size are input to the shared parameter network MLP at the same time. Finally, the new feature map output from the shared parameter network is subjected to a summation operation and a sigmoid activation function to obtain the channel attention features ({M}_{c}).The channel attention module CAM is calculated as shown in Formula (1):$${text{M}}_{rm{c}}({text{F}}){=sigma}({text{MLP (AvgPool (F))}}+ {text MLP (MaxPool (F)))}{=sigma}({rm{W}}_{1}({text{W}}_{0}({text{F}}_{{{rm{avg}}}^{rm{c}}}))+{rm{W}}_{0}({rm{W}}_{1}({rm{F}}_{{{rm{max}}}^{rm{c}}})))$$
    (1)
    where σ represents the sigmoid function, MLP represents the shared parameter network, ({text{W}}_{0}) and ({text{W}}_{1}) represent the shared weights, ({text{F}}_{text{avg}}^{text{c}}) is the result of feature map F after global average pooling, and ({text{F}}_{text{max}}^{text{c}}) is the result of feature map F after global maximum pooling.The working principle of SAM is shown in Fig. 4c. The feature map F’ is regarded as the input of the SAM. F’ is obtained by multiplying the input of SAM with the output of CAM. First, the global maximum pooling operation and the global average pooling operation are applied to the channels of the feature map to obtain two feature maps of the same size. Second, two feature maps that have completed the pooling operation are stitched at the channels and the feature channels are dimensioned down using the convolution operation to obtain a new feature map. Finally, spatial attention features ({text{M}}_{text{s}}) are generated using the sigmoid activation function.The spatial attention module (SAM) is calculated, as shown in Formula (2):$${text{M}}_{text{s}}left({text{F}}right) {=sigma}left({text{f}}^{7 times 7}left(left[{text{AvgPool}}left({text{F}}right)text{;MaxPool}left({text{F}}right)right]right)right) {=sigma}left({text{f}}^{7 times 7}left(left[{text{F}}_{text{avg}}^{text{s}} ; {text{F}}_{text{max}}^{text{s}}right]right)right)$$
    (2)
    where σ is the sigmoid function, ({text{f}}^{7 times 7}) denotes the convolution operation with a filter size of 7 × 7, ({text{F}}_{text{avg}}^{text{s}}) is the result of the feature map after global average pooling, and ({text{F}}_{text{max}}^{text{s}}) is the result of the feature map after global maximum pooling.Squeeze and excitation networkIn 2018, Hu et al.27 proposed a single-path attention network structure SE-Net. SE-Net uses the idea of an attention mechanism to analyze the relationship feature maps by modeling and adaptively learning to obtain the importance of each feature map28 and then assigns different weights to the original feature map for updating according to the importance. In this way, SE-Net pays more attention to the features that are useful for the target task while suppressing useless feature information and allocates computational resources rationally to different channels to train the model to achieve better results.The SE-Net attention module is mainly composed of two parts: the squeeze operation and excitation operation. The structure of the SE-Net module is shown in Fig. 5.Figure 5The SE-Net module structure.Full size imageThe squeeze operation uses global average pooling to encode all spatial features on the channel as local features. Second, each feature map is compressed into a real number that has global information on the feature maps. Finally, the squeeze results of each feature map are combined into a vector as the weights of each group of feature maps. It is calculated as shown in Eq. (3):$${text{Z}}_{text{c}}={text{F}}_{text{sq}}left({text{u}}_{text{c}}right)=frac{1}{text{H} times {text{W}}}sum_{text{i=1}}^{text{H}}sum_{text{j=1}}^{text{W}}{{text{u}}}_{text{c}}left(text{i,j}right) , , , $$
    (3)
    where H is the height of the feature map, W is the feature map width, u is the result after convolution, z is the global attention information of the corresponding feature map, and the subscript c indicates the number of channels.After completing the squeeze operation to obtain the channel information, the feature vector is subjected to the excitation operation. First, it passes through two fully connected layers. Second, it uses the sigmoid function. Finally, the output weights are assigned to the original features. It is calculated as follows:$$text{s} = {text{F}}_{text{ex}}left(text{z,W}right){=sigma}left({text{g}}left(text{z,W}right)right){=sigma}left({text{W}}_{2}{delta}left({text{W}}_{1}{text{z}}right)right)$$
    (4)
    $$widetilde{{text{x}}_{rm{c}}}={text{F}}_{rm{scale}}left({text{u}}_{rm{c}}, {text{s}}_{rm{c}}right)={text{s}}_{rm{c}}{{text{u}}}_{rm{c}}$$
    (5)
    where σ is the ReLU activation function, δ represents the sigmoid activation function, and ({text{W}}_{1}) and ({text{W}}_{2}) represent two different fully connected layers. The vector s represents the set of feature mapping weights obtained through the fully connected layer and the activation function. (widetilde{{x}_{c}}) is the feature mapping of the x feature channel, ({text{s}}_{text{c}}) is a weight, and ({text{u}}_{text{c}}) is a two-dimensional matrix.Target detection layerThe garbage in rural areas is a smaller target and has fewer pixel characteristics, such as capsule, button butteries. Therefore, we insert a small target detection layer to improve the head network structure based on the original YOLOv5s network model for detecting objects with small targets to optimize the problem of missed detection in the original network model. The YOLOv5s network structure with the addition of the small target detection layer is shown in Fig. 6 and named YOLOv5s-STD.Figure 6The YOLOv5s-STD network structure.Full size imageIn the seventeenth layer of the neck network, operations such as upsampling are performed on the feature maps so that the feature maps continue to expand. Meanwhile, in the twentieth layer, the feature maps obtained from the neck network are fused with the feature maps extracted from the backbone network. We insert a detection layer capable of predicting small targets in the thirty-first layer. To improve the detection accuracy, we use a total of four detection layers for the output feature maps, which are capable of detecting smaller target objects. In addition to the three initial anchor values based on the original model, an additional set of anchor values is added as a way to detect smaller targets. The anchor values of the improved YOLOv5s network model are set to [5, 6, 8, 14, 15, 11], [10, 13, 16, 30, 33, 23], [30, 61, 62, 45, 59, 119] and [116, 90, 156, 198, 373, 326].Bounding box regression loss functionThe loss function is an important indicator of the generalization ability of a model. In 2016, Yu et al.29 proposed a new joint intersection loss function IoU for bounding box prediction. IoU stands for intersection over union, which is a frequently used metric in target detection. It is used not only to determine the positive and negative samples, but also to determine the similarity between the predicted bounding box and the ground truth bounding box. It can be described as shown in the Eq. (6):$$text{IoU} = frac{left|text{A} capleft.{text{B}}right|right.}{left|{text{A}} cupleft.{text{B}}right|right.}$$
    (6)
    where the value domain of IoU ranges from [0,1]. A and B are the areas of arbitrary regions. Additionally, when IoU is used as a loss function, it has to scale invariance, as shown in Eq. (7):$$text{IoU_Loss} = 1-frac{left|text{A} cap left.{text{B}}right|right.}{left|{text{A}} cup left.{text{B}}right|right.}$$
    (7)
    However, when the prediction bounding box and the ground truth bounding box do not intersect, namely IoU = 0, the distance between the arbitrary region area of A and B cannot be calculated. The loss function at this point is not derivable and cannot be used to optimize the two disjoint bounding boxes. Alternatively, when there are different intersection positions, where the overlapping parts are the same but in different overlapping directions, the IoU loss function cannot be predicted.To address these issues, the idea of GIoU (Generalized Intersection over Union)30, in which a minimum rectangular Box C of A and B is added, was proposed in 2019 by Rezatofighi et al. Suppose the prediction bounding box is B, the ground truth bounding box is A, the area where A and B intersect is D, and the area containing two bounding boxes is C, as shown in Fig. 7.Figure 7GIoU evaluation chart.Full size imageThen, the GIoU calculation, as shown in Formula (8), is:$$text{GIoU}= text{IoU}-frac{text{|C}-left({text{A}} cup {text{B}}right)text{|}}{text{|C|}}$$
    (8)
    The GIoU_Loss is calculated as (9):$$text{GIoU_Loss=1}-{text{IoU}}-frac{text{|C}-left({text{A}} cup {text{B}}right)text{|}}{text{|C|}}$$
    (9)
    The original YOLOv5 algorithm uses GIoU_Loss as the loss function. Comparing Eqs. (6) and (8), it can be seen that GIoU is a new penalty term (frac{text{|C}-left({text{A}} cup {text{B}}right)text{|}}{text{|C|}}) that is added to IoU and is clearly represented by Fig. 7.Although the GIoU loss function solves the problem that the gradient of the IoU loss function cannot be updated in time and the prediction bounding box, the direction of the ground truth bounding box is not consistent when predicting, but there are still disadvantages, as shown in Fig. 8.Figure 8Comparsion of loss values.Full size imageFigure 8 shows three different position relationships formed when the predicted bounding box and the ground truth bounding box overlap exactly. Among them, the ratio of the length to width of the green grounding truth bounding box is 1:2, and the red predicted bounding box has the same aspect ratio as the ground truth bounding box, but the size is only one-half of the green ground truth bounding box. When the prediction bounding box and the ground truth bounding box completely overlap, the GIoU degenerates to the IoU, and the GIoU value and IoU value for the three different position cases are 0.45 at this time. The GIoU loss function does not directly reflect the distance between the prediction bounding box and the ground truth bounding box. Therefore, we introduce the CIoU (Complete Intersection over Union)31 loss function to replace the original GIoU loss function in the YOLOv5 algorithm and continue to optimize the prediction bounding box.Therefore, the CIoU is calculated as (10):$$text{GIoU_Loss}=1-text{IoU}-frac{text{|C}-left({text{A}} cup {text{B}}right)text{|}}{text{|C|}}$$
    (10)
    where b and ({text{b}}^{text{gt}}) denote the centroids of the prediction bounding box and the ground truth bounding box, respectively, ({rho}) is the Euclidean distance between the two centroids, and c is the diagonal length of the minimum closed area formed by the prediction bounding box and the ground truth bounding box.(alpha) is the parameter used to balance the scale, and v is the scale consistency used to measure the aspect ratio between the prediction bounding box and the ground truth bounding box, as shown in Eqs. (11) and (12).$$alpha =frac{text{v}}{left(1-text{IoU}right)+{text{v}}^{{prime}}}$$
    (11)
    $$text{v} = frac{4}{{pi}^{2}}{left({text{arctan}}frac{{omega}^{text{gt}}}{{text{h}}^{text{gt}}}- text{arctan}frac{{omega}^{text{p}}}{{text{h}}^{text{p}}}right)}^{2}$$
    (12)
    Therefore, the expression of CIoU_Loss can be obtained according to Eqs. (10), (11) and (12).$$text{CIoU_Loss} =1-text{CIoU}=1-text{IoU}+frac{{rho}^{2}left(text{b,}{text{b}}^{text{gt}}right)}{{text{c}}^{2}}{+ alpha v }$$
    (13)
    Optimization algorithmAfter optimizing the loss function of the network model, the next step is to optimize the hyperparameters of the network model. The function of the optimizer is to adjust the hyperparameters to the most appropriate values while making the loss function converge as much as possible32. In the target detection algorithm, the optimizer is mainly used to calculate the gradient of the loss function and to iteratively update the parameters.The optimizer used in YOLOv5 is stochastic gradient descent (SGD). Since a large number of problems in deep learning satisfy the strict saddle function, all the local optimal solutions obtained are almost as ideal. Therefore, SGD algorithm is not trapped in the saddle point and has strong generality. However, the slow convergence speed and the number of iterations of SGD algorithm are still problems that need to be improved. Adam algorithm has both the first-order momentum in the SGD algorithm and combines the second-order momentum in AdaGrad algorithm and AdaDelta algorithm, Adaptive&Momentum. Adam formula can be described as follows:$${m}_{t}={beta }_{1}{m}_{t-1}+left(1-{beta }_{1}right){g}_{t}$$
    (14)
    $${v}_{t}={beta }_{2}{v}_{t-1}+left(1-{beta }_{2}right){g}_{t}^{2}$$
    (15)
    $${widehat{m}}_{t}=frac{{m}_{t}}{1-{beta }_{1}^{t}}$$
    (16)
    $${widehat{v}}_{t}=frac{{v}_{t}}{1-{beta }_{2}^{t}}$$
    (17)
    where ({beta }_{1}) and ({beta }_{2}) parameters are hyperparameters and g is the current gradient value of the error function, ({m}_{t}) is the gradient of the first-order momentum and ({v}_{t}) is the gradient of the second-order momentum.Adam is an adaptive one-step random objective function optimization algorithm based on a low-order moment. It can replace the traditional first-order optimization algorithm for the stochastic gradient descent process. It is able to update the weights of the neural network adaptively based on the data trained during the iterative process. The Adam optimizer occupies fewer memory resources during the training process and is suitable for solving the problems of sparse gradients and large fluctuations in loss values33. Therefore, we use the Adam optimization algorithm instead of the SGD optimization algorithm to train the network model based on the YOLOv5s network model. The calculation is shown in Table 3.Table 3 Computing method of the Adam optimizer.Full size tablewhere ({alpha}) is a factor controlling the learning rate of the network, ({beta}^{{prime}}) is the exponential decay rate of the first-order moment estimate, ({beta}^{{primeprime}}) is the exponential decay rate of the second-order moment estimate, and ({varepsilon}) is a constant that tends to zero infinitely as the denominator. More

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    Applying genomic approaches to delineate conservation strategies using the freshwater mussel Margaritifera margaritifera in the Iberian Peninsula as a model

    Funk, W. C., McKay, J. K., Hohenlohe, P. A. & Allendorf, F. W. Harnessing genomics for delineating conservation units. Trends Ecol. Evol. 27, 489–496. https://doi.org/10.1016/j.tree.2012.05.012 (2012).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Hohenlohe, P. A., Funk, W. C. & Rajora, O. P. Population genomics for wildlife conservation and management. Mol. Ecol. 30, 62–82. https://doi.org/10.1111/mec.15720 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Helyar, S. J. et al. Application of SNPs for population genetics of nonmodel organisms: New opportunities and challenges. Mol. Ecol. Resour. 11, 123–136. https://doi.org/10.1111/j.1755-0998.2010.02943.x (2011).ADS 
    Article 
    PubMed 

    Google Scholar 
    Allendorf, F. W. Genetics and the conservation of natural populations: Allozymes to genomes. Mol. Ecol. 26, 420–430. https://doi.org/10.1111/mec.13948 (2017).CAS 
    Article 
    PubMed 

    Google Scholar 
    Zimmerman, S. J., Aldridge, C. L. & Oyler-McCance, S. J. An empirical comparison of population genetic analyses using microsatellite and SNP data for a species of conservation concern. BMC Genomics 21, 38. https://doi.org/10.1186/s12864-020-06783-9 (2020).CAS 
    Article 

    Google Scholar 
    Lemopoulos, A. et al. Comparing RADseq and microsatellites for estimating genetic diversity and relatedness—implications for brown trout conservation. Ecol. Evol. 9, 2106–2120. https://doi.org/10.1002/ece3.4905 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kleinman-Ruiz, D. et al. Novel efficient genome-wide SNP panels for the conservation of the highly endangered Iberian lynx. BMC Genomics 18, 556. https://doi.org/10.1186/s12864-017-3946-5 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Geist, J. Strategies for the conservation of endangered freshwater pearl mussels (Margaritifera margaritifera L.): A synthesis of conservation genetics and ecology. Hydrobiologia 644, 69–88. https://doi.org/10.1007/s10750-010-0190-2 (2010).Lopes-Lima, M. et al. Conservation status of freshwater mussels in Europe: State of the art and future challenges. Biol. Rev. 92, 572–607. https://doi.org/10.1111/brv.12244 (2017).Article 
    PubMed 

    Google Scholar 
    Outeiro, A., Ondina, P., Fernández, C., Amaro, R. & Miguel, E. S. Population density and age structure of the freshwater Pearl mussel, Margaritifera margaritifera, in two Iberian rivers. Freshw. Biol. 53, 485–496. https://doi.org/10.1111/j.1365-2427.2007.01913.x (2008).CAS 
    Article 

    Google Scholar 
    Clements, E. A., Thomas, R. & Adams, C. E. An investigation of salmonid host utilisation by the endangered freshwater pearl mussel (Margaritifera margaritifera) in north-west Scotland. Aquat. Conserv.: Mar. Freshw. Ecosyst. 28, 764–768. https://doi.org/10.1002/aqc.2900 (2018).Taeubert, J-E. & Geist, J. The relationship between the Freshwater Pearl Mussel (Margaritifera margaritifera) and its hosts. Biol. Bull. 44, 67–73. https://doi.org/10.1134/S1062359017010149 (2017).Sousa, R. et al. Conservation status of the freshwater pearl mussel Margaritifera margaritifera in Portugal. Limnologica 50, 4–10. https://doi.org/10.1016/j.limno.2014.07.004 (2015).Article 

    Google Scholar 
    Almodóvar, A., Nicola, G. G., Ayllón, D. & Elvira, B. Global warming threatens the persistence of Mediterranean brown trout. Glob. Change Biol. 18, 1549–1560. https://doi.org/10.1111/j.1365-2486.2011.02608.x (2012).ADS 
    Article 

    Google Scholar 
    Nicola, G. G., Elvira, B., Johnson, B., Ayllón, D. & Almodóvar, A. Local and global climatic drivers of Atlantic salmon decline in southern Europe. Fish. Res. 198, 78–85. https://doi.org/10.1016/j.fishres.2017.10.012 (2018).Article 

    Google Scholar 
    da Silva, J. P. et al. Predicting climatic threats to an endangered freshwater mussel in Europe: The need to account for fish hosts. Freshw. Biol. 00, 1–15. https://doi.org/10.1111/fwb.13885 (2022).Article 

    Google Scholar 
    Strayer, D. L., Geist, J., Haag, W. R., Jackson, J. K. & Newbold, J. D. Essay: Making the most of recent advances in freshwater mussel propagation and restoration. Conserv. Sci. Pract. 43, e53. https://doi.org/10.1111/csp2.53 (2009).Article 

    Google Scholar 
    Geist, J., Bayerl, H., Stoeckle, B. C. & Kuehn, R. Securing genetic integrity in freshwater pearl mussel propagation and captive breeding. Sci. Rep. 11, 16019. https://doi.org/10.1038/s41598-021-95614-2 (2021).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gomes dos Santos, A. et al. The Crown Pearl: a draft genome assembly of the European freshwater pearl mussel Margaritifera margaritifera (Linnaeus, 1758). DNA Res. 28, dsab002. https://doi.org/10.1093/dnares/dsab002 (2021).Bouza, C. et al. Threatened freshwater pearl mussel Margaritifera margaritifera L. in NW Spain: low and very structured genetic variation in southern peripheral assessed using microsatellite markers. Conserv. Genet. 8: 937–948. https://doi.org/10.1007/s10592-006-9248-0 (2007).Stoeckle, B. C. et al. Strong genetic differentiation and low genetic diversity of the freshwater pearl mussel (Margaritifera margaritifera L.) in the southwestern European distribution range. Conserv. Genet. 18, 147–157. https://doi.org/10.1007/s10592-016-0889-3 (2017).Geist, J., Söderberg, H., Karllberg, A. & Kuehn, R. Drainage-independent genetic structure and high genetic diversity of endangered freshwater pearl mussels (Margaritifera margaritifera) in northern Europe. Conserv. Genet. 11, 1339–1350. https://doi.org/10.1007/s10592-009-9963-4 (2010).Article 

    Google Scholar 
    implications for conservation and management. Geist, J. & Kuehn, R. Genetic diversity and differentiation of central European freshwater pearl mussel (Margaritifera margaritifera L.) populations. Mol. Ecol. 14, 239–425. https://doi.org/10.1111/j.1365-294X.2004.02420.x (2005).CAS 
    Article 

    Google Scholar 
    Farrington, S. J., King, R. W., Baker, J. A. & Gibbons, J. G. Population genetics of freshwater pearl mussel (Margaritifera margaritifera) in central Massachusetts and implications for conservation. Aquat. Conserv.: Mar. Freshw. Ecosyst. 30, 1945–1958. https://doi.org/10.1002/aqc.3439 (2020).Zanatta, D. T. et al. High genetic diversity and low differentiation in North American Margaritifera margaritifera (Bivalvia: Unionida: Margaritiferidae). Biol. J. Linn. Soc. Lond., 123, 850–863. https://doi.org/10.1093/biolinnean/bly010. (2018)Garrison, N. L., Johnson, P. D. & Whelan, N. V. Conservation genomics reveals low genetic diversity and multiple parentage in the threatened freshwater mussel Margaritifera hembeli. Conser. Genet. 22, 217–231. https://doi.org/10.1007/s10592-020-01329-8 (2021).Article 

    Google Scholar 
    Roe, K. & Kim, K. S. Genome-wide SNPs redefine species-boundaries and conservation units in the freshwater mussel genus Cyprogenia of North America. Sci. Rep. 11, 10752. https://doi.org/10.1038/s41598-021-90325-0 (2021).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wingett, S. W. & Andrews, S. FastQ Screen: A tool for multi-genome mapping and quality control. F1000Res 7, 1338. https://doi.org/10.12688/f1000research.15931.2 (2018).Ewels, P., Magnusson, M., Lundin, S. & Käller, M. MultiQC: Summarize analysis results for multiple tools and samples in a single report. Bioinformatics 32, 3047–3048. https://doi.org/10.1093/bioinformatics/btw354 (2016).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    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. https://doi.org/10.1111/mec.15253 (2019).CAS 
    Article 
    PubMed 

    Google Scholar 
    Paris, R. J., Stevens, J. R. & Catchen, J. M. Lost in parameter space: A road map for STACKS. Methods Ecol. Evol. 8, 1360–1373. https://doi.org/10.1111/2041-210X.12775 (2017).Article 

    Google Scholar 
    Limin, F., Niu, B., Zhu, Z., Wu, S. & Li, W. CD-HIT: Accelerated for clustering the next-generation sequencing data. Bioinformatics 28, 3150–3152. https://doi.org/10.1093/bioinformatics/bts565 (2012).CAS 
    Article 

    Google Scholar 
    Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv:1303.3997v2. https://doi.org/10.48550/arXiv.1303.3997 (2013).Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079. https://doi.org/10.1093/bioinformatics/btp352 (2009).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Garrison E, Marth G. Haplotype-based variant detection from short-read sequencing. arXiv:1207.3907v2. https://doi.org/10.48550/arXiv.1207.3907 (2012)Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158. https://doi.org/10.1093/bioinformatics/btr330 (2011).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Excoffier, L. & Lischer, H. E. L. Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10, 564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x (2010).Weir, B. S. & Cockerham, C. Estimating F-statistics for the analysis of population structure. Evol. 38, 1358–1370. https://doi.org/10.2307/2408641 (1984).CAS 
    Article 

    Google Scholar 
    Frichot, E. & François, O. LEA: An R package for landscape and ecological association studies. Methods Ecol. Evol. 6, 925–929. https://doi.org/10.1111/2041-210X.12382 (2015).Article 

    Google Scholar 
    Alexander, D. H, Novembre, J. & Lange, K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655–1664. https://doi.org/10.1101/gr.094052.109 (2009).Jakobsson, M. & Rosenberg, N. A. CLUMPP: A cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801–1806. https://doi.org/10.1093/bioinformatics/btm233 (2007).CAS 
    Article 
    PubMed 

    Google Scholar 
    Frankham, R. et al. A practical guide for genetic management of fragmented animal and plant populations. Oxford University Press, New York. 174. https://doi.org/10.1093/oso/9780198783411.001.0001 (2019).Wacker, S., Larson, B., Jakobsen, P. & Karlssona, S. Multiple paternity promotes genetic diversity in captive breeding of a freshwater mussel. Glob. Ecol. Cons. 17, e00564. https://doi.org/10.1016/j.gecco.2019.e00564 (2019).Article 

    Google Scholar 
    Cao, R. et al. Genetic structure and diversity of Australian freshwater crocodiles (Crocodylus johnstoni) from the Kimberley Western Australia. Conserv. Genet. 21, 421–429. https://doi.org/10.1007/s10592-020-01259-5 (2020).Article 

    Google Scholar 
    Escalante, M. A. et al. Genotyping-by-sequencing reveals the effects of riverscape, climate and interspecific introgression on the genetic diversity and local adaptation of the endangered Mexican Golden trout (Oncorhynchus chrysogaster). Conserv. Genet. 21, 907–926. https://doi.org/10.1371/journal.pone.0141775 (2020).CAS 
    Article 

    Google Scholar 
    Bauer, G. Reproductive strategy of the freshwater pearl mussel Margaritifera margaritifera. J. Anim. Ecol. 56, 691–704. https://doi.org/10.2307/5077 (1987).Article 

    Google Scholar 
    Machordom, A., Araujo, R., Erpenbeck, D. & Ramos, M. A. Phylogeography and conservation genetics of endangered European Margaritiferidae (Bibalvia: Unionoidae). Biol. J. Linn. Soc. 78, 235–252. https://doi.org/10.1046/j.1095-8312.2003.00158.x (2003).Article 

    Google Scholar 
    Viveen, W., Schoorl, J. M., Veldkamp, A., van Balen, R. T. & Vidal-Romani, J. R. Fluvial terraces of the northwest Iberian lower Miño River. J. Maps 9, 513–522. https://doi.org/10.1080/17445647.2013.821096 (2013).Article 

    Google Scholar 
    Pérez-Granados, C., López-Iborra, G. & Seoane, J. A multi-scale analysis of habitat selection in peripheral populations of the endangered Dupont’s Lark Chersophilus duponti. Bird Conserv. Intern. 27, 398–413. https://doi.org/10.1017/S0959270916000356 (2017).Article 

    Google Scholar 
    Sanz Ball-Llosera, N., Garcìa-Marìn, J. & Pla, C. Managing fish populations under mosaic relationships. The case of brown trout (Salmo trutta) in peripheral Mediterranean populations. Conserv. Genet. 3, 385–400. https://doi.org/10.1023/A:1020527420654 (2002).Vila, M. et al. Phylogeography and Conservation Genetics of the Ibero-Balearic Three-Spined Stickleback (Gasterosteus aculeatus). PLoS One 12, e0170685. https://doi.org/10.1371/journal.pone.0170685 (2017)Hamed, Y. et al. Climate impacto n Surface and groundwater in North Africa: A global synthesis of findings and recommendations. Euro-Mediterr. J. Environ. Integr. 3, 25. https://doi.org/10.1007/s41207-018-0067-8 (2018).Article 

    Google Scholar 
    Krijgsman, W. et al. The Gibraltar Corridor: Watergate of the Messinian Salinity Crisis. Mar. Geol. 403, 238–246. https://doi.org/10.1016/j.margeo.2018.06.008 (2018).ADS 
    Article 

    Google Scholar 
    Zanatta, D. T. & Wilson, C. C. Testing congruency of geographic and genetic population structure for a freshwater mussel Bivalvia: Unionoida) and its host fish. Biol. J. Linn. Soc. 102, 669–685. https://doi.org/10.1111/j.1095-8312.2010.01596.x (2011).Article 

    Google Scholar 
    Österling, E. M., Ferm, J. & Piccolo, J.J. Parasitic freshwater pearl mussel larvae (Margaritifera margaritifera L.) reduce the drift-feeding rate of juvenile brown trout (Salmo trutta L.). Environ. Biol. Fish. 97, 543–549. https://doi.org/10.1007/s10641-014-0251-x (2014).Geist, J. et al. Genetic structure of Irish freshwater pearl mussels (Margaritifera margaritifera and Margaritifera durrovensis): Validity of subspecies, roles of host fish, and conservation implications. Aquat. Conserv. Mar. Freshw. Ecosyst. 28, 923–933. https://doi.org/10.1002/aqc.2913 (2018)Wacker, S., Larsen, B. M., Karlsson, S. & Hindar, K. Host specificity drives genetic structure in a freshwater mussel. Sci. Rep. 9, 10409 (2019).Machordom, A., Suárez, J., Almodóvar, A. & Bautista, J. Mitochondrial haplotype variation and phylogeography of Iberian brown trout populations. Mol. Ecol. 9, 1325–1338. https://doi.org/10.1046/j.1365-294x.2000.01015.x (2000).CAS 
    Article 

    Google Scholar 
    Suárez, J., Bautista, J. M., Almodóvar, A. & Machordom, A. Evolution of the mitocondrial control region in Paleartic brown trout (Salmo trutta) populations: The biogeographical role of the Iberian Peninsula. Heredity 87, 198–206. https://doi.org/10.1046/j.1365-2540.2001.00905.x (2001).Article 
    PubMed 

    Google Scholar 
    Velasco, J. C. et al. Descubiertos algunos ejemplares de Margaritifera margaritifera (L.) (Bivalvia, Unionoida) en el alto Duero (Soria, España). Iberus 32(2), 97–104 (2014).Geist, J. & Kuehn, R. Host-parasite interactions in oligotrophic stream ecosystems: the roles of life history strategy and ecological niche. Mol. Ecol. 17, 997–1008. https://doi.org/10.1111/j.1365-294X.2007.03636.x. (2008)Ledoux, J.-B., et al. Gradients of genetic diversity and differentiation across the distribution range of a Mediterranean coral: Patterns, processes and conservation implications. Divers. Distrib. 27, 2104–2123 https://doi.org/10.1111/ddi.13382 (2021).Hervella F, & Caballero P. Inventario piscícola dos ríos galegos. Consellería de Medio Ambiente. Xunta de Galicia. Santiago de Compostela (1999).Saura, M., Caballero, P. & Morán, P. Are there Atlantic salmon in the River Tambre?. J. Fish Biol. 72, 1223–1229. https://doi.org/10.1111/j.1095-8649.2007.01782.x (2008).Article 

    Google Scholar 
    Hoban, S. et al. Genetic diversity targets and indicators in the CBD post-2020 global biodiversity framework must be improved. Biol. Conserv. 248, 108654. https://doi.org/10.1016/j.biocon.2020.108654 (2020).Article 

    Google Scholar 
    Rilov, G. et al. Adaptive marine conservation planning in the face of climate change: What can we learn from physiological, ecological and genetic studies?. Glob. Ecol. Conserv. 17, e00566. https://doi.org/10.1016/j.gecco.2019.e00566 (2019).Article 

    Google Scholar 
    Muniz, F. L. et al. Delimitation of evolutionary units in Cuvier’s dwarf caiman, Paleosuchus palpebrosus (Cuvier, 1807): Insights from conservation of a broadly distributed species. Conserv. Genet. 19, 599–610. https://doi.org/10.1007/s10592-017-1035-6 (2018).Article 

    Google Scholar 
    Gum, B., Lange, M. & Geist, J. A critical reflection on the success of rearing and culturing of juvenile freshwater mussels with a focus on the endangered freshwater pearl mussel (Margaritifera margaritifera L.). Aquat. Conserv. 21, 743–751. https://doi.org/10.1002/aqc.1222 (2011).Thomas, G. R., Taylor, J. & García de Leaniz, C. Captive breeding of the endangered freshwater Pearl mussel Margaritifera margaritifera. Endanger. Species Res. 12, 1–9. https://doi.org/10.3354/esr00286 (2010).Wilson, C. D. et al. The importance of population genetic information in formulating ex situ conservation strategies for the freshwater pearl mussel (Margaritifera margaritifera L.) in Northern Ireland. Anim. Conserv. 15, 595–602. https://doi.org/10.1111/j.1469-1795.2012.00553.x (2012).Pires, D., Reis, J., Benites, L. & Rodrigues, P. Minimizing dams impacts on biodiversity by way of translocations: the case of freshwater mussels. Impact Assess. Proj. Apprais. 39, 110–117. https://doi.org/10.1080/14615517.2020.1836710. (2021) More