Philippa Kaur

McCave IN. Vertical flux of particles in the ocean. Deep-Sea Res. 1975;22:491–502.
Google Scholar 
Ducklow HW, Steinberg DK, Buesseler KO. Upper ocean carbon export and the biological pump. Oceanography. 2001;14:50–8.
Google Scholar 
Siegenthaler U, Sarmiento JL. Atmospheric carbon dioxide and the ocean. Nature 1993;365:119–25.CAS 

Google Scholar 
Bar-On YM, Phillips R, Milo R. The biomass distribution on Earth. Proc Natl Acad Sci USA. 2018;115:6506–11.CAS 
PubMed 
PubMed Central 

Google Scholar 
Turley CM, Mackie PJ. Biogeochemical significance of attached and free-living bacteria and the flux of particles in the NE Atlantic Ocean. Mar Ecol Prog Ser. 1994;115:191–204.
Google Scholar 
Turley CM, Stutt ED. Depth-related cell-specific bacterial leucine incorporation rates on particles and its biogeochemical significance in the Northwest Mediterranean. Limnol Oceanogr. 2000;45:419–25.CAS 

Google Scholar 
Aristegui J, Gasol JM, Duarte CM, Herndl GJ. Microbial oceanography of the dark ocean’s pelagic realm. Limnol Oceanogr. 2009;54:1501–29.CAS 

Google Scholar 
Fontanez KM, Eppley JM, Samo TJ, Karl DM, DeLong EF. Microbial community structure and function on sinking particles in the North Pacific Subtropical Gyre. Front Microbiol. 2015;6:469.PubMed 
PubMed Central 

Google Scholar 
Pelve EA, Fontanez KM, DeLong EF. Bacterial succession on sinking particles in the ocean’s interior. Front Microbiol. 2017;8:2669.
Google Scholar 
Boeuf D, Edwards BR, Eppley JM, Hu SK, Poff KE, Romano AE, et al. Biological composition and microbial dynamics of sinking particulate organic matter at abyssal depths in the oligotrophic open ocean. Proc Natl Acad Sci USA. 2019;116:11824–32.CAS 
PubMed 
PubMed Central 

Google Scholar 
Preston CM, Durkin CA, Yamahara KM. DNA metabarcoding reveals organisms contributing to particulate matter flux to abyssal depths in the North East Pacific ocean. Deep-Sea Res Part II. 2020;173:104708.CAS 

Google Scholar 
Mestre M, Ruiz-González C, Logares R, Duarte CM, Gasol JM, Sala MM. Sinking particles promote vertical connectivity in the ocean microbiome. Proc Natl Acad Sci USA. 2018;115:E6799–807.CAS 
PubMed 
PubMed Central 

Google Scholar 
Jiao N, Herndl GJ, Hansell DA, Benner R, Kattner G, Wilhelm SW, et al. Microbial production of recalcitrant dissolved organic matter: Long-term carbon storage in the global ocean. Nat Rev Microbiol. 2010;8:593–9.CAS 
PubMed 

Google Scholar 
Poff KE, Leu AO, Eppley JM, Karl DM, DeLong EF. Microbial dynamics of elevated carbon flux in the open ocean’s abyss. Proc Natl Acad Sci USA. 2021;118:1–11.
Google Scholar 
DeLong EF, Franks DG, Alldredge AL. Phylogenetic diversity of aggregate‐attached vs. free‐living marine bacterial assemblages. Limnol Oceanogr. 1993;38:924–34.
Google Scholar 
Rieck A, Herlemann DPR, Jürgens K, Grossart HP. Particle-associated differ from free-living bacteria in surface waters of the Baltic Sea. Front Microbiol. 2015;6:1297.PubMed 
PubMed Central 

Google Scholar 
Crespo BG, Pommier T, Fernández-Gómez B, Pedrós-Alió C. Taxonomic composition of the particle-attached and free-living bacterial assemblages in the Northwest Mediterranean Sea analyzed by pyrosequencing of the 16S rRNA. Microbiologyopen. 2013;2:541–52.CAS 
PubMed 
PubMed Central 

Google Scholar 
Eloe EA, Shulse CN, Fadrosh DW, Williamson SJ, Allen EE, Bartlett DH. Compositional differences in particle-associated and free-living microbial assemblages from an extreme deep-ocean environment. Environ Microbiol Rep. 2011;3:449–58.PubMed 

Google Scholar 
Ghiglione JF, Mevel G, Pujo-Pay M, Mousseau L, Lebaron P, Goutx M. Diel and seasonal variations in abundance, activity, and community structure of particle-attached and free-living bacteria in NW Mediterranean Sea. Micro Ecol. 2007;54:217–31.CAS 

Google Scholar 
López-Pérez M, Kimes NE, Haro-Moreno JM, Rodriguez-Valera F. Not all particles are equal: The selective enrichment of particle-associated bacteria from the Mediterranean Sea. Front Microbiol. 2016;7:996.PubMed 
PubMed Central 

Google Scholar 
Farnelid H, Turk-Kubo K, Ploug H, Ossolinski JE, Collins JR, Van Mooy BAS, et al. Diverse diazotrophs are present on sinking particles in the North Pacific Subtropical Gyre. ISME J. 2019;13:170–82.PubMed 

Google Scholar 
Mende DR, Boeuf D, DeLong EF. Persistent core populations shape the microbiome throughout the water column in the North Pacific Subtropical Gyre. Front Microbiol. 2019;10:1–12.
Google Scholar 
Proctor LM, Fuhrman JA. Roles of viral infection in organic particle flux. Mar Ecol Prog Ser. 1991;69:133–42.
Google Scholar 
Peduzzi P, Weinbauer MG. Effect of concentrating the virus‐rich 2‐2nm size fraction of seawater on the formation of algal flocs (marine snow). Limnol Oceanogr. 1993;38:1562–5.
Google Scholar 
Weinbauer MG. Ecology of prokaryotic viruses. FEMS Microbiol Rev. 2004;28:127–81.CAS 
PubMed 

Google Scholar 
Zimmerman AE, Howard-Varona C, Needham DM, John SG, Worden AZ, Sullivan MB, et al. Metabolic and biogeochemical consequences of viral infection in aquatic ecosystems. Nat Rev Microbiol. 2019;18:21–34.PubMed 

Google Scholar 
Wilhelm SW, Suttle CA. Viruses and nutrient cycles in the sea. Bioscience. 1999;49:781–8.
Google Scholar 
Gobler CJ, Hutchins DA, Fisher NS, Cosper EM, Sañudo-Wilhelmy SA. Release and bioavailability of C, N, P, Se, and Fe following viral lysis of a marine chrysophyte. Limnol Oceanogr. 1997;42:1492–504.CAS 

Google Scholar 
Middelboe M, Jørgensen NOG, Kroer N. Effects of viruses on nutrient turnover and growth efficiency of noninfected marine bacterioplankton. Appl Environ Microbiol. 1996;62:1991–7.CAS 
PubMed 
PubMed Central 

Google Scholar 
Alldredge AL, Silver MW. Characteristics, dynamics and significance of marine snow. Prog Oceanogr. 1988;20:41–82.
Google Scholar 
Shibata A, Kogure K, Koike I, Ohwada K. Formation of submicron colloidal particles from marine bacteria by viral infection. Mar Ecol Prog Ser. 1997;155:303–7.
Google Scholar 
Yamada Y, Tomaru Y, Fukuda H, Nagata T. Aggregate formation during the viral lysis of a marine diatom. Front Mar Sci. 2018;5:1–7.
Google Scholar 
Lawrence JE, Suttle CA. Effect of viral infection on sinking rates of Heterosigma akashiwo and its implications for bloom termination. Aquat Micro Ecol. 2004;37:1–7.
Google Scholar 
Michaels A, Silver M. Primary production, sinking fluxes and the microbial food web. Deep-Sea Res. Part I 1988;35:473–90.
Google Scholar 
Richardson TL. Mechanisms and pathways of small-phytoplankton export from the surface ocean. Ann Rev Mar Sci. 2019;11:57–74.PubMed 

Google Scholar 
Richardson T, Jackson GA. Small phytoplankton and carbon export from the surface ocean. Science. 2007;315:838–40.CAS 
PubMed 

Google Scholar 
Lomas MW, Moran SB. Evidence for aggregation and export of cyanobacteria and nano-eukaryotes from the Sargasso Sea euphotic zone. Biogeosciences 2011;8:203–16.CAS 

Google Scholar 
Liu H, Nolla HA, Campbell L. Prochlorococcus growth rate and contribution to primary production in the equatorial and subtropical North Pacific Ocean. Aquat Micro Ecol. 1997;12:39–47.
Google Scholar 
Kaneko H, Blanc-Mathieu R, Endo H, Chaffron S, Delmont TO, Gaia M, et al. Eukaryotic virus composition can predict the efficiency of carbon export in the global ocean. iScience. 2021;24:102002.Guidi L, Chaffron S, Bittner L, Eveillard D, Larhlimi A, Roux S, et al. Plankton networks driving carbon export in the oligotrophic ocean. Nature 2015;532:465–70.
Google Scholar 
Laber CP, Hunter JE, Carvalho F, Collins JR, Hunter EJ, Schieler BM, et al. Coccolithovirus facilitation of carbon export in the North Atlantic. Nat Microbiol. 2018;3:537–47.CAS 
PubMed 

Google Scholar 
Sheyn U, Rosenwasser S, Lehahn Y, Barak-Gavish N, Rotkopf R, Bidle KD, et al. Expression profiling of host and virus during a coccolithophore bloom provides insights into the role of viral infection in promoting carbon export. ISME J. 2018;12:704–13.CAS 
PubMed 
PubMed Central 

Google Scholar 
Karl DM, Church MJ. Microbial oceanography and the Hawaii Ocean Time-series programme. Nat Rev Microbiol. 2014;12:1–15.
Google Scholar 
Karl DM, Church MJ, Dore JE, Letelier RM, Mahaffey C. Predictable and efficient carbon sequestration in the North Pacific Ocean supported by symbiotic nitrogen fixation. Proc Natl Acad Sci USA. 2012;109:1842–9.CAS 
PubMed 
PubMed Central 

Google Scholar 
Karl DM, Lukas R. The Hawaii Ocean Time-series (HOT) program: Background, rationale and field implementation. Deep-Sea Res Part II. 1996;43:129–56.CAS 

Google Scholar 
Roux S, Enault F, Hurwitz BL, Sullivan MB. VirSorter: mining viral signal from microbial genomic data. PeerJ. 2015;3:e985.PubMed 
PubMed Central 

Google Scholar 
Kieft K, Zhou Z, Anantharaman K. VIBRANT: automated recovery, annotation and curation of microbial viruses, and evaluation of viral community function from genomic sequences. Microbiome 2020;8:90.CAS 
PubMed 
PubMed Central 

Google Scholar 
Arumugam M, Harrington ED, Raes J, Foerstner KU, Arumugam M, Bork P. SmashCommunity: A metagenomic annotation and analysis tool. Bioinformatics. 2010;26:2977–8.CAS 
PubMed 

Google Scholar 
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19:455–77.CAS 
PubMed 
PubMed Central 

Google Scholar 
Roux S, Emerson JB, Eloe-Fadrosh EA, Sullivan MB. Benchmarking viromics: An in silico evaluation of metagenome-enabled estimates of viral community composition and diversity. PeerJ. 2017;5:e3817.PubMed 
PubMed Central 

Google Scholar 
Hyatt D, Chen G, Locascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: Prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics. 2010;11:119.Eddy SR. Accelerated Profile HMM Searches. PLoS Comput Biol. 2011;7:e1002195.CAS 
PubMed 
PubMed Central 

Google Scholar 
Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, Hotz H, et al. The Pfam protein families database. Nucleic Acids Res. 2008;36:281–8.Li W, Godzik A. Cd-hit: A fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics. 2006;22:1658–9.CAS 
PubMed 

Google Scholar 
Mizuno CM, Guyomar C, Roux S, Lavigne R, Rodriguez-Valera F, Sullivan M, et al. Numerous cultivated and uncultivated viruses encode ribosomal proteins. Nat Commun. 2019;10:752.CAS 
PubMed 
PubMed Central 

Google Scholar 
Kielbasa SM, Wan R, Sato K, Kiebasa SM, Horton P, Frith MC. Adaptive seeds tame genomic sequence comparison. Genome Res. 2011;21:487–93.CAS 
PubMed 
PubMed Central 

Google Scholar 
Nishimura Y, Watai H, Honda T, Mihara T, Omae K, Roux S, et al. Environmental viral genomes shed new light on virus-host interactions in the ocean. mSphere. 2017;2:e00359–16.CAS 
PubMed 
PubMed Central 

Google Scholar 
Imai T sprai = single pass read accuracy improver [Internet]. 2013. Available from: http://zombie.cb.k.u-tokyo.ac.jp/sprai/Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, et al. Versatile and open software for comparing large genomes. Genome Biol. 2004;5:R12.PubMed 
PubMed Central 

Google Scholar 
Beaulaurier J, Luo E, Eppley JM, Uyl PDen, Dai X, Burger A, et al. Assembly-free single-molecule sequencing recovers complete virus genomes from natural microbial communities. Genome Res. 2020;30:437–46.CAS 
PubMed 
PubMed Central 

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

Google Scholar 
Skennerton CT, Imelfort M, Tyson GW. Crass: Identification and reconstruction of CRISPR from unassembled metagenomic data. Nucleic Acids Res. 2013;41:e105.CAS 
PubMed 
PubMed Central 

Google Scholar 
O’Leary NA, Wright MW, Brister JR, Ciufo S, Haddad D, Mcveigh R, et al. Reference sequence (RefSeq) database at NCBI: Current status, taxonomic expansion, and functional annotation. Nucleic Acids Res. 2016;44:733–45. (Database issue)
Google Scholar 
Luo E, Eppley JM, Romano AE, Mende DR, DeLong EF. Double-stranded DNA virioplankton dynamics and reproductive strategies in the oligotrophic open ocean water column. ISME J. 2020;14:1304–15.CAS 
PubMed 
PubMed Central 

Google Scholar 
Mizuno CM, Rodriguez-Valera F, Kimes NE, Ghai R. Expanding the marine virosphere using metagenomics. PLoS Genet. 2013;9:e1003987.PubMed 
PubMed Central 

Google Scholar 
Mizuno CM, Ghai R, Saghaï A, López-García P, Rodriguez-Valera F. Genomes of abundant and widespread viruses from the deep ocean. MBio. 2016;7:e00805–16.CAS 
PubMed 
PubMed Central 

Google Scholar 
Roux S, Brum JR, Dutilh BE, Sunagawa S, Duhaime MB, Loy A, et al. Ecogenomics and biogeochemical impacts of uncultivated globally abundant ocean viruses. Nature. 2016;537:689–93.CAS 
PubMed 

Google Scholar 
Paez-Espino D, Eloe-Fadrosh EA, Pavlopoulos GA, Thomas AD, Huntemann M, Mikhailova N, et al. Uncovering Earth’s virome. Nature. 2016;536:425–30.CAS 
PubMed 

Google Scholar 
López-Pérez M, Haro-Moreno JM, Gonzalez-Serrano R, Parras-Moltó M, Rodriguez-Valera F. Genome diversity of marine phages recovered from Mediterranean metagenomes: Size matters. PLoS Genet. 2017;13:1–23.
Google Scholar 
Coutinho FH, Silveira CB, Gregoracci GB, Thompson CC, Edwards RA, Brussaard CPD, et al. Marine viruses discovered via metagenomics shed light on viral strategies throughout the oceans. Nat Commun. 2017;8:15955.CAS 
PubMed 
PubMed Central 

Google Scholar 
Gregory AC, Zayed AA, Sunagawa S, Wincker P, Sullivan MB, Ferland J, et al. Marine DNA viral macro- and microdiversity from pole to pole. Cell. 2019;177:1–15.
Google Scholar 
Luo E, Aylward FO, Mende DR, Delong EF. Bacteriophage distributions and temporal variability in the ocean’s interior. MBio. 2017;8:e01903–17.CAS 
PubMed 
PubMed Central 

Google Scholar 
Eren AM, Esen ÖC, Quince C, Vineis JH, Morrison HG, Sogin ML, et al. Anvi’o: An advanced analysis and visualization platform for ‘omics data. PeerJ. 2015;3:e1319.PubMed 
PubMed Central 

Google Scholar 
Langfelder P, Horvath S. WGCNA: An R package for weighted correlation network analysis. BMC Bioinformatics. 2008;9:559.R Core Team. R: A Language and Environment for Statistical Computing [Internet]. Vienna, Austria; 2019. Available from: https://www.r-project.org/Lauro FM, Chastain RA, Blankenship LE, Yayanos AA, Bartlett DH. The unique 16S rRNA genes of piezophiles reflect both phylogeny and adaptation. Appl Environ Microbiol. 2007;73:838–45.CAS 
PubMed 

Google Scholar 
DeLong EF, Franks DG, Yayanos AA. Evolutionary relationships of cultivated psychrophilic and barophilic deep-sea bacteria. Appl Environ Microbiol. 1997;63:2105–8.CAS 
PubMed 
PubMed Central 

Google Scholar 
Berg KA, Lyra C, Sivonen K, Paulin L, Suomalainen S, Tuomi P, et al. High diversity of cultivable heterotrophic bacteria in association with cyanobacterial water blooms. ISME J. 2009;3:314–25.CAS 
PubMed 

Google Scholar 
Rii YM, Karl DM, Church MJ. Temporal and vertical variability in picophytoplankton primary productivity in the North Pacific Subtropical Gyre. Mar Ecol Prog Ser. 2016;562:1–18.CAS 

Google Scholar 
Martin JH, Knauer GA, Karl DM, Broenkow WW. VERTEX: Carbon cycling in the northeast Pacific. Deep-Sea Res. 1987;34:267–85.CAS 

Google Scholar 
Karl MD, Knauer AG. Detritus-microbe interactions in the marine pelagic environment: Selected results from the vertex experiment. Bull Mar Sci. 1984;35:550–65.
Google Scholar 
Scanlan DJ, Ostrowski M, Mazard S, Dufresne A, Garczarek L, Hess WR, et al. Ecological genomics of marine picocyanobacteria. Microbiol Mol Biol Rev. 2009;73:249–99.CAS 
PubMed 
PubMed Central 

Google Scholar 
McDonnell AMP, Boyd PW, Buesseler KO. Effects of sinking velocities and microbial respiration rates on the attenuation of particulate carbon fluxes through the mesopelagic zone. Glob Biogeochem Cycles. 2015;29:175–93.CAS 

Google Scholar 
Qiu B, Koh DA, Lumpkin C, Flament P. Existence and formation mechanism of the North Hawaiian Ridge Current. J Phys Oceanogr. 1997;27:431–44.
Google Scholar 
Turner JT. Zooplankton fecal pellets, marine snow, phytodetritus and the ocean’s biological pump. Prog Oceanogr. 2015;130:205–48.
Google Scholar  More

Bennett, A. F. Linkages in the Landscape The Role of Corridors and Connectivity in Wildlife Conservation. (IUCN, Gland, Switzerland and Cambridge, UK).Berger, J., Young, J. K. & Berger, K. M. Protecting migration corridors: Challenges and optimism for Mongolian Saiga. PLOS Biol. 6, e165 (2008).PubMed 
PubMed Central 

Google Scholar 
Murphy, S. M. et al. Consequences of severe habitat fragmentation on density, genetics, and spatial capture-recapture analysis of a small bear population. PLOS ONE 12, 1–20 (2017).
Google Scholar 
Kaboodvandpour, S., Almasieh, K. & Zamani, N. Habitat suitability and connectivity implications for the conservation of the Persian leopard along the Iran-Iraq border. Ecol. Evol. 11, 13464–13474 (2021).PubMed 
PubMed Central 

Google Scholar 
Hilty, J. A., Lidicker, W. Z. Jr. & Merenlender, A. M. Corridor Ecology: The Science and Practice of Linking Landscapes for Biodiversity Conservation (Island Press, Washington DC, 2012).
Google Scholar 
Noss, R. F., Quigley, H. B., Hornocker, M. G., Merrill, T. & Paquet, P. C. Conservation biology and carnivore conservation in the rocky mountains. Conserv. Biol. 10, 949–963 (1996).
Google Scholar 
Terraube, J., Van Doninck, J., Helle, P. & Cabeza, M. Assessing the effectiveness of a national protected area network for carnivore conservation. Nat. Commun. 11, 1–9 (2020).
Google Scholar 
Ashrafzadeh, M. R. et al. A multi-scale, multi-species approach for assessing effectiveness of habitat and connectivity conservation for endangered felids. Biol. Conserv. 245, 108523 (2020).
Google Scholar 
Mohammadi, A. et al. Identifying priority core habitats and corridors for effective conservation of brown bears in Iran. Sci. Rep. 11, 1–13 (2021).MathSciNet 

Google Scholar 
Beier, P., Majka, D. R. & Spencer, W. D. Forks in the road: Choices in procedures for designing wildland linkages. Conserv. Biol. 22, 836–851 (2008).PubMed 

Google Scholar 
Calvignac, S., Hughes, S. & Hänni, C. Genetic diversity of endangered brown bear (ursus arctos) populations at the crossroads of Europe, Asia and Africa. Divers. Distrib. 15, 742–750 (2009).
Google Scholar 
Khosravi, R., Hemami, M. R. & Cushman, S. A. Multi-scale niche modeling of three sympatric felids of conservation importance in central Iran. Landsc. Ecol. 34, 2451–2467 (2019).
Google Scholar 
Almasieh, K., Rouhi, H. & Kaboodvandpour, S. Habitat suitability and connectivity for the brown bear (Ursus arctos) along the Iran-Iraq border. Eur. J. Wildl. Res. 65, 1–12 (2019).
Google Scholar 
Balme, G. A., Hunter, L. T. B. & Slotow, R. Evaluating methods for counting cryptic carnivores. J. Wildl. Manage. 73, 433–441 (2009).
Google Scholar 
Guisan, A. & Zimmermann, N. E. Predictive habitat distribution models in ecology. Ecol. Modell. 135, 147–186 (2000).
Google Scholar 
McRae, B. H. & Beier, P. Circuit theory predicts gene flow in plant and animal populations. Proc. Natl. Acad. Sci. USA 104, 19885–19890 (2007).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Farhadinia, M. S. et al. Leveraging trans-boundary conservation partnerships: Persistence of Persian leopard (Panthera pardus saxicolor) in the Iranian Caucasus. Biol. Conserv. 191, 770–778 (2015).
Google Scholar 
Almasieh, K., Mirghazanfari, S. M. & Mahmoodi, S. Biodiversity hotspots for modeled habitat patches and corridors of species richness and threatened species of reptiles in central Iran. Eur. J. Wildl. Res. 65, 1–13 (2019).
Google Scholar 
Mohammadi, A. et al. Road expansion: A challenge to conservation of mammals, with particular emphasis on the endangered Asiatic cheetah in Iran. J. Nat. Conserv. 43, 8–18 (2018).
Google Scholar 
Cushman, S. A., Lewis, J. S. & Landguth, E. L. Evaluating the intersection of a regional wildlife connectivity network with highways. Mov. Ecol. 1, 1–11 (2013).
Google Scholar 
Mohammadi, A. & Fatemizadeh, F. Quantifying landscape degradation following construction of a highway using landscape metrics in Southern Iran. Front. Ecol. Evol. 9, 836 (2021).
Google Scholar 
Crooks, K. R. Relative sensitivities of mammalian carnivores to habitat fragmentation. Conserv. Biol. 16, 488–502 (2002).
Google Scholar 
Moqanaki, E. M. & Cushman, S. A. All roads lead to Iran: Predicting landscape connectivity of the last stronghold for the critically endangered Asiatic cheetah. Anim. Conserv. 20, 29–41 (2017).
Google Scholar 
Neumann, W. et al. Difference in spatiotemporal patterns of wildlife road-crossings and wildlife-vehicle collisions. Biol. Conserv. 145, 70–78 (2012).
Google Scholar 
Mohammadi, A. & Kaboli, M. Evaluating wildlife-vehicle collision hotspots using kernel-based estimation: A focus on the endangered Asiatic cheetah in central Iran. Human-Wildlife Interact. 10, 103–109 (2016).
Google Scholar 
Benítez-López, A., Alkemade, R. & Verweij, P. A. The impacts of roads and other infrastructure on mammal and bird populations: A meta-analysis. Biol. Conserv. 143, 1307–1316 (2010).
Google Scholar 
Dadashi-Jourdehi, A., Shams-Esfandabad, B., Ahmadi, A., Rezaei, H. R. & Toranj-Zar, H. Predicting the potential distribution of striped hyena Hyaena hyaena in Iran. Belgian J. Zool. 150, 185–195 (2020).
Google Scholar 
Akay, A. E., Inac, S. & Yildirim, I. C. Monitoring the local distribution of striped hyenas (Hyaena hyaena L.) in the Eastern Mediterranean Region of Turkey (Hatay) by using GIS and remote sensing technologies. Environ. Monit. Assess. 181, 445–455 (2011).PubMed 

Google Scholar 
AbiSaid, M. & Dloniak, S. M. D. Hyaena hyaena. The IUCN Red List of Threatened Species 2015. (2015).Alam, M. S. & Khan, J. A. Food habits of striped hyena (Hyaena hyaena) in a semi-arid conservation area of India. J. Arid Land 7, 860–866 (2015).
Google Scholar 
Wagner, A. P. Behavioral ecology of the striped hyena (Hyaena hyaena). ProQuest Diss. Theses 195–195 (2006).Hofer, H. Species Accounts, Status Survey and Conservation Action Plan of Hyaena (Information Press, 1998).
Google Scholar 
Kruuk, H. Feeding and social behaviour of the striped hyaena (Hyaena vulgaris Desmarest). East African Wildl. J. 14, 91–111 (1976).
Google Scholar 
Tourani, M., Moqanaki, E. M. & Kiabi, B. H. Vulnerability of striped hyaenas, hyaena hyaena, in a human-dominated landscape of central Iran. Zool. Middle East 56, 133–136 (2012).
Google Scholar 
Parchizadeh, J. & Belant, J. L. Human-caused mortality of large carnivores in Iran during 1980–2021. Glob. Ecol. Conserv. 27, e01618 (2021).
Google Scholar 
Almasieh, K., Zoratipour, A., Negaresh, K. & Delfan-Hasanzadeh, K. Habitat quality modelling and effect of climate change on the distribution of Centaurea pabotii in Iran. Spanish J. Agric. Res. 16, e0304 (2018).
Google Scholar 
Ahmadi, M. et al. Species and space: A combined gap analysis to guide management planning of conservation areas. Landsc. Ecol. 35, 1505–1517 (2020).
Google Scholar 
Yusefi, G. H., Faizolahi, K., Darvish, J., Safi, K. & Brito, J. C. The species diversity, distribution, and conservation status of the terrestrial mammals of Iran. J. Mammal. 100, 55–71 (2019).
Google Scholar 
Karami, M., Ghadirian, T. & Faizolahi, K. The atlas of mammals of Iran ; Jahad daneshgahi, kharazmi Branch (Department of the Environment of Iran, 2016).Singh, P., Gopalaswamy, A. M. & Karanth, K. U. Factors influencing densities of striped hyenas (Hyaena hyaena) in arid regions of India. J. Mammal. 91, 1152–1159 (2010).
Google Scholar 
Brown, J. L. SDMtoolbox: A python-based GIS toolkit for landscape genetic, biogeographic and species distribution model analyses. Methods Ecol. Evol. 5, 694–700 (2014).
Google Scholar 
Esri. ArcGIS 10.1. Environ. Syst. Res. Institute, Redlands, CA, USA (2012).Rieger, I. A review of the biology of striped hyaenas, Hyaena hyaena (Linne, 1758). Saugetierkund. Mitt. 27, 81–95 (1979).
Google Scholar 
Jueterbock, A. ‘ MaxentVariableSelection ’ vignette (2015).Team, R. C. R: A language and environment for statistical computing. R Foundation for Statistical Computing. (2019).Naimi, B., Hamm, N. A. S., Groen, T. A., Skidmore, A. K. & Toxopeus, A. G. Where is positional uncertainty a problem for species distribution modelling?. Ecography (Cop.) 37, 191–203 (2014).
Google Scholar 
Zuur, A. F., Ieno, E. N. & Elphick, C. S. A protocol for data exploration to avoid common statistical problems. Methods Ecol. Evol. 1, 3–14 (2010).
Google Scholar 
Thuiller, W., Lafourcade, B., Engler, R. & Araújo, M. B. BIOMOD: A platform for ensemble forecasting of species distributions. Ecography (Cop.) 32, 369–373 (2009).
Google Scholar 
Shahnaseri, G. et al. Contrasting use of habitat, landscape elements, and corridors by grey wolf and golden jackal in central Iran. Landsc. Ecol. 34, 1263–1277 (2019).
Google Scholar 
Araújo, M. B. & New, M. Ensemble forecasting of species distributions. Trends Ecol. Evol. 22, 42–47 (2007).PubMed 

Google Scholar 
Eskildsen, A. et al. Testing species distribution models across space and time: high latitude butterflies and recent warming. Glob. Ecol. Biogeogr. 22, 1293–1303 (2013).
Google Scholar 
Wan, H. Y., Cushman, S. A. & Ganey, J. L. Improving habitat and connectivity model predictions with multi-scale resource selection functions from two geographic areas. Landsc. Ecol. 34, 503–519 (2019).
Google Scholar 
Mateo-Sánchez, M. C. et al. A comparative framework to infer landscape effects on population genetic structure: Are habitat suitability models effective in explaining gene flow?. Landsc. Ecol. 30, 1405–1420 (2015).
Google Scholar 
Landguth, E. L., Hand, B. K., Glassy, J., Cushman, S. A. & Sawaya, M. A. UNICOR: A species connectivity and corridor network simulator. Ecography (Cop.) 35, 9–14 (2012).
Google Scholar 
Cushman, S. A., McKelvey, K. S. & Schwartz, M. K. Use of empirically derived source-destination models to map regional conservation corridors. Conserv. Biol. 23(2), 368–376 (2009).PubMed 

Google Scholar 
Saura, S. & Torné, J. Conefor Sensinode 2.2: A software package for quantifying the importance of habitat patches for landscape connectivity. Environ. Model. Softw. 24, 135–139 (2009).
Google Scholar 
Saura, S. & Pascual-Hortal, L. A new habitat availability index to integrate connectivity in landscape conservation planning: Comparison with existing indices and application to a case study. Landsc. Urban Plan. 83, 91–103 (2007).
Google Scholar 
Saura, S. & Rubio, L. A common currency for the different ways in which patches and links can contribute to habitat availability and connectivity in the landscape. Ecography (Cop.) 33, 523–537 (2010).
Google Scholar 
Avon, C. & Bergès, L. Prioritization of habitat patches for landscape connectivity conservation differs between least-cost and resistance distances. Landsc. Ecol. 31, 1551–1565 (2016).
Google Scholar 
Cushman, S. A., Lewis, J. S. & Landguth, E. L. Why did the bear cross the road? Comparing the performance of multiple resistance surfaces and connectivity modeling methods. Diversity 6, 844–854 (2014).
Google Scholar 
Mohammadi, A. et al. Integrating spatial analysis and questionnaire survey to better understand human-onager conflict in Southern Iran. Sci. Rep. 11, 1–12 (2021).MathSciNet 

Google Scholar 
Shamoon, H. & Shapira, I. Limiting factors of Striped Hyaena, Hyaena hyaena, distribution and densities across climatic and geographical gradients (Mammalia: Carnivora). Zool. Middle East 65, 189–200 (2019).
Google Scholar 
Leakey, L. N. et al. Diet of striped hyaena in northern Kenya. Afr. J. Ecol. 37, 314–326 (1999).
Google Scholar 
Farhadinia, M. S., Johnson, P. J., Hunter, L. T. B. & Macdonald, D. W. Wolves can suppress goodwill for leopards: Patterns of human-predator coexistence in northeastern Iran. Biol. Conserv. 213, 210–217 (2017).
Google Scholar 
Bhandari, S., Bhusal, D. R., Psaralexi, M. & Sgardelis, S. Habitat preference indicators for striped hyena (Hyaena hyaena) in Nepal. Glob. Ecol. Conserv. 27, e01619 (2021).
Google Scholar 
Farashi, A. & Shariati, M. Biodiversity hotspots and conservation gaps in Iran. J. Nat. Conserv. 39, 37–57 (2017).
Google Scholar 
Farashi, A., Shariati, M. & Hosseini, M. Identifying biodiversity hotspots for threatened mammal species in Iran. Mamm. Biol. 87, 71–88 (2017).
Google Scholar 
Boitani, L., Ciucci, P., Corsi, F. & Dupre, E. Range and corridors for brown bears in the eastern potential. Ursus 11, 123–130 (1999).
Google Scholar 
Bhandari, S., Morley, C., Aryal, A. & Shrestha, U. B. The diet of the striped hyena in Nepal’s lowland regions. Ecol. Evol. 10, 7953–7962 (2020).PubMed 
PubMed Central 

Google Scholar  More

Winston, M. R. & Taylor, C. M. Upstream extirpation of four minnow species due to damming of a prairie stream. Trans. Am. Fish. Soc. 120, 8 (1991).
Google Scholar 
Graham, K. Contemporary status of the North American paddlefish, Polyodon spathula. Environ. Biol. Fishes 48, 279–289 (1997).
Google Scholar 
Kaushal, S. S. et al. Rising stream and river temperatures in the United States. Front. Ecol. Environ. 8, 461–466 (2010).
Google Scholar 
Vörösmarty, C. J. et al. Global threats to human water security and river biodiversity. Nature 467, 555–561 (2010).PubMed 
ADS 

Google Scholar 
Galbreath, P. F., Bisbee, M. A., Dompier, D. W., Kamphaus, C. M. & Newsome, T. H. Extirpation and tribal reintroduction of coho salmon to the interior columbia river basin. Fisheries 39, 77–87 (2014).
Google Scholar 
Schmidt, B. A. et al. Determining habitat limitations of Maumee River walleye production to western Lake Erie fish stocks: Documenting a spawning ground barrier. J. Gt. Lakes Res. 46, 1661–1673 (2020).
Google Scholar 
Kendall, N. W., Marston, G. W. & Klungle, M. M. Declining patterns of Pacific Northwest steelhead trout (Oncorhynchus mykiss) adult abundance and smolt survival in the ocean. Can. J. Fish. Aquat. Sci. 74, 1275–1290 (2017).
Google Scholar 
Myers, J., Bryant, G. & Lynch, J. Factors Contributing to the Decline of Chinook Salmon: An Addendum to the 1996 West Coast Steelhead Factors for Decline Report (Springer, 1998).
Google Scholar 
Molony, B. W., Lenanton, R., Jackson, G. & Norriss, J. Stock enhancement as a fisheries management tool. Rev. Fish Biol. Fish. 13, 409–432 (2005).
Google Scholar 
Merz, J. E. & Setka, J. D. Evaluation of a spawning habitat enhancement site for Chinook salmon in a regulated California river. N. Am. J. Fish. Manag. 24, 397–407 (2004).
Google Scholar 
Ostberg, C. O., Chase, D. M. & Hauser, L. Hybridization between yellowstone cutthroat trout and rainbow trout alters the expression of muscle growth-related genes and their relationships with growth patterns. PLoS ONE 10, e0141373 (2015).PubMed 
PubMed Central 

Google Scholar 
Veale, A. J. & Russello, M. A. Sockeye salmon repatriation leads to population re-establishment and rapid introgression with native kokanee. Evol. Appl. 9, 1301–1311 (2016).CAS 
PubMed 
PubMed Central 

Google Scholar 
Fraser, D. J., Cook, A. M., Eddington, J. D., Bentzen, P. & Hutchings, J. A. Mixed evidence for reduced local adaptation in wild salmon resulting from interbreeding with escaped farmed salmon: Complexities in hybrid fitness. Evol. Appl. 1, 501–512 (2008).PubMed 
PubMed Central 

Google Scholar 
Stewart, G. S. et al. The power of evolutionary rescue is constrained by genetic load. Evol. Appl. 10, 731–741 (2017).PubMed 
PubMed Central 

Google Scholar 
Weeks, A. R. et al. Genetic rescue increases fitness and aids rapid recovery of an endangered marsupial population. Nat. Commun. 8, 1071 (2017).PubMed 
PubMed Central 
ADS 

Google Scholar 
Chan, W. Y., Hoffmann, A. A. & van Oppen, M. J. H. Hybridization as a conservation management tool. Conserv. Lett. 12, e12652 (2019).
Google Scholar 
Bekkevold, D., Hansen, M. M. & Nielsen, E. E. Genetic impact of gadoid culture on wild fish populations: Predictions, lessons from salmonids, and possibilities for minimizing adverse effects. ICES J. Mar. Sci. 63, 198–208 (2006).
Google Scholar 
Muhlfeld, C. C. et al. Hybridization rapidly reduces fitness of a native trout in the wild. Biol. Lett. 5, 328–331 (2009).PubMed 
PubMed Central 

Google Scholar 
Harvey, A. C., Glover, K. A., Taylor, M. I., Creer, S. & Carvalho, G. R. A common garden design reveals population-specific variability in potential impacts of hybridization between populations of farmed and wild Atlantic salmon, Salmo salar L. Evol. Appl. 9, 435–449 (2016).PubMed 
PubMed Central 

Google Scholar 
Edmands, S. Does parental divergence predict reproductive compatibility?. Trends Ecol. Evol. 17, 520–527 (2002).
Google Scholar 
Johnson, B. M., Johnson, M. S. & Thorgaard, G. H. Salmon genetics and management in the Columbia river basin. Northwest Sci. 92, 346–363 (2019).
Google Scholar 
Hanson, A. J. & Smith, H. D. Mate selection in a population of sockeye salmon (Oncorhynchus nerka) of mixed age-groups. J. Fish. Board Can. 24, 23 (1967).
Google Scholar 
Wood, C. C. & Foote, C. J. Evidence for sympatric genetic divergence of anadromous and nonanadromous morphs of sockeye salmon (Oncorhynchus nerka). Evolution 50, 1265–1279 (1996).PubMed 

Google Scholar 
Foote, C. J. Male mate choice dependent on male size in salmon. Behaviour 106, 63–80 (1988).
Google Scholar 
Craig, J. K., Foote, C. J. & Wood, C. C. Countergradient variation in carotenoid use between sympatric morphs of sockeye salmon (Oncorhynchus nerka) exposes nonanadromous hybrids in the wild by their mismatched spawning colour. Biol. J. Linn. Soc. 84, 287–305 (2005).
Google Scholar 
Taylor, E. B. & Foote, C. J. Critical swimming velocities of juvenile sockeye salmon and kokanee, the anadromous and non-anadromous forms of Oncorhynchus nerka (Walbaum). J. Fish Biol. 38, 407–419 (1991).
Google Scholar 
Foote, C. J., Wood, C. C., Clarke, W. C. & Blackburn, J. Circannual cycle of seawater adaptability in Oncorhynchus nerka: Genetic differences between sympatric sockeye salmon and kokanee. Can. J. Fish. Aquat. Sci. 49, 99–109 (1992).
Google Scholar 
Wood, C. C. & Foote, C. J. Genetic differences in the early development and growth of sympatric sockeye salmon and kokanee (Oncorhynchus nerka), and their hybrids. Can. J. Fish. Aquat. Sci. 47, 2250–2260 (1990).
Google Scholar 
Elliott, L. D., Ward, H. G. M. & Russello, M. A. Kokanee–sockeye salmon hybridization leads to intermediate morphology and resident life history: Implications for fisheries management. Can. J. Fish. Aquat. Sci. 77, 355–364 (2020).
Google Scholar 
Hendry, A. P., Quinn, T. P. & Utter, F. M. Genetic evidence for the persistence and divergence of native and introduced sockeye salmon (Oncorhynchus nerka) within Lake Washington, Washington. Can. J. Fish. Aquat. Sci. 53, 823–832 (1996).
Google Scholar 
Praebel, K. et al. A diagnostic tool for efficient analysis of the population structure, hybridization and conservation status of European whitefish (Coregonus lavaretus (L.)) and vendace (C. albula (L.)). Adv. Limnol. 64, 247–255 (2013).
Google Scholar 
Sanz, N., Araguas, R. M., Fernández, R., Vera, M. & García-Marín, J.-L. Efficiency of markers and methods for detecting hybrids and introgression in stocked populations. Conserv. Genet. 10, 225–236 (2009).CAS 

Google Scholar 
Mcfarlane, S. & Pemberton, J. Detecting the true extent of introgression during anthropogenic hybridization. Trends Ecol. Evol. 34, 315–326 (2019).PubMed 

Google Scholar 
Vähä, J.-P. & Primmer, C. R. Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Mol. Ecol. 15, 63–72 (2006).PubMed 

Google Scholar 
Boecklen, W. J. & Howard, D. J. Genetic analysis of hybrid zones: Numbers of markers and power of resolution. Ecology 78, 2611–2616 (1997).
Google Scholar 
Elliott, L. & Russello, M. A. SNP panels for differentiating advanced-generation hybrid classes in recently diverged stocks: A sensitivity analysis to inform monitoring of sockeye salmon re-stocking programs. Fish. Res. 208, 339–345 (2018).
Google Scholar 
Twyford, A. D. & Ennos, R. A. Next-generation hybridization and introgression. Heredity 108, 179–189 (2012).CAS 
PubMed 

Google Scholar 
Campbell, N. R., Harmon, S. A. & Narum, S. R. Genotyping-in-Thousands by sequencing (GT-seq): A cost effective SNP genotyping method based on custom amplicon sequencing. Mol. Ecol. Resour. 15, 855–867 (2015).CAS 
PubMed 

Google Scholar 
Alexander, C. A. & Pickard, D. Skaha Lake Experimental Sockeye Reintroduction: Synthesis of First 4 of 12 Years (2004–2007 Brood Years) (Springer, 2009).
Google Scholar 
McQueen, D. et al. Evaluation of the Experimental Introduction of Sockeye Salmon (Oncorhynchus nerka) into Skaha Lake and Assessment of Sockeye Rearing in Osoyoos Lake (Springer, 2013).
Google Scholar 
Hegg, J. C., Kennedy, B. P. & Chittaro, P. What did you say about my mother? The complexities of maternally derived chemical signatures in otoliths. Can. J. Fish. Aquat. Sci. 76, 81–94 (2019).CAS 

Google Scholar 
Veale, A. J. & Russello, M. A. Genomic changes associated with reproductive and migratory ecotypes in sockeye salmon (Oncorhynchus nerka). Genome Biol. Evol. 9, 2921–2939 (2017).CAS 
PubMed 
PubMed Central 

Google Scholar 
Catchen, J., Hohenlohe, P. A., Bassham, S., Amores, A. & Cresko, W. A. Stacks: An analysis tool set for population genomics. Mol. Ecol. 22, 3124–3140 (2013).PubMed 
PubMed Central 

Google Scholar 
Hohenlohe, P. A., Amish, S. J., Catchen, J. M., Allendorf, F. W. & Luikart, G. Next-generation RAD sequencing identifies thousands of SNPs for assessing hybridization between rainbow and westslope cutthroat trout. Mol. Ecol. Resour. 11, 117–122 (2011).PubMed 

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

Google Scholar 
Weir, B. S. & Cockerham, C. C. Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370 (1984).CAS 
PubMed 

Google Scholar 
Rousset, F. genepop’007: A complete re-implementation of the genepop software for Windows and Linux. Mol. Ecol. Resour. 8, 103–106 (2008).PubMed 

Google Scholar 
Anderson, E. C. & Thompson, E. A. A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160, 1217–1229 (2002).CAS 
PubMed 
PubMed Central 

Google Scholar 
Schmidt, D. A., Campbell, N. R., Govindarajulu, P., Larsen, K. W. & Russello, M. A. Genotyping-in-Thousands by sequencing (GT-seq) panel development and application to minimally invasive DNA samples to support studies in molecular ecology. Mol. Ecol. Resour. 20, 114–124 (2020).CAS 
PubMed 

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

Google Scholar 
Reeves, P. A., Bowker, C. L., Fettig, C. E., Tembrock, L. R. & Richards, C. M. Effect of Error and Missing Data on Population Structure Inference Using Microsatellite Data. (2016) https://doi.org/10.1101/080630.Wringe, B. F., Stanley, R. R. E., Jeffery, N. W., Anderson, E. C. & Bradbury, I. R. hybriddetective: A workflow and package to facilitate the detection of hybridization using genomic data in r. Mol. Ecol. Resour. 17, e275–e284 (2017).CAS 
PubMed 

Google Scholar 
Walsh, P. S., Metzger, D. A. & Higuchi, R. Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10, 506–513 (1991).CAS 
PubMed 

Google Scholar 
Russell, T. et al. Development of a novel mule deer genomic assembly and species-diagnostic SNP panel for assessing introgression in mule deer, white-tailed deer, and their interspecific hybrids. Genes Genomes Genet. 9, 911–919 (2019).CAS 

Google Scholar 
Thongda, W. et al. Species-diagnostic SNP markers for the black basses (Micropterus spp.): A new tool for black bass conservation and management. Conserv. Genet. Resour. 12, 319–328 (2020).
Google Scholar 
Ricker, W. E. ‘Residual’ and kokanee salmon in Cultus lake. J. Fish. Board Can. 27, 192–218 (1938).
Google Scholar 
Crossin, G. T. et al. Exposure to high temperature influences the behaviour, physiology, and survival of sockeye salmon during spawning migration. Can. J. Zool. 86, 127–140 (2008).CAS 

Google Scholar 
Moore, M. E. et al. Early marine migration patterns of wild coastal cutthroat trout (Oncorhynchus clarkii clarkii), steelhead trout (Oncorhynchus mykiss), and their hybrids. PLoS ONE 5, e12881 (2010).PubMed 
PubMed Central 
ADS 

Google Scholar 
McCutcheon, C. S., Prentice, E. F. & Park, D. L. Passive monitoring of migrating adult steelhead with PIT tags. N. Am. J. Fish. Manag. 14, 220–223 (1994).
Google Scholar 
Scribner, K. T., Page, K. S. & Bartron, M. L. Hybridization in freshwater fishes: A review of case studies and cytonuclear methods of biological inference. Rev. Fish Biol. Fish. 10, 293–323 (2001).
Google Scholar  More

Field collectionEndophytic fungi and insects were assessed from dormant twig samples from 155 tree species at 51 locations in 32 countries. Sampled tree species belonged to genera that are native to, and occur widely across, either the northern or southern hemisphere, since very few tree genera occur naturally in both hemispheres (e.g., in our study only Podocarpus appears in both hemispheres but has a limited distribution in the northern hemisphere). We sampled largely in botanical gardens and arboreta, which allowed us to sample native and non-native, congeneric and confamiliar, tree species at each location. At each location, one native and one to three non-native congeneric or confamiliar tree species were sampled.At each location, twenty 50-cm long asymptomatic twigs were collected from 1–5 individual trees per species, from different branches and different parts of the crown (Fig. 1). The number of individual trees per species depended on the number of trees available in the specific botanical garden or arboretum, which was often low (Table 1). All twigs per tree species and location were pooled and analysed as a single sample. On some occasions two samples of the same tree species at the same location are considered. Sampling was conducted in the month with the shortest day-length in the year (end of December 2017 in the Northern hemisphere, end of June 2018 in the Southern hemisphere). Samples originating from a tropical region (eleven samples from Tanzania) were collected in June 2018. Trees were sampled in winter to align with the timing of trade, i.e. most woody plants are traded in winter or early spring, as plants will be planted in the following spring, and to reduce the risk of introducing foliar pests in deciduous trees. Evergreen gymnosperm and angiosperm tree species, which were also considered, do not lose foliage during winter, and are thus sold with leaves/needles.Table 1 Site information for sampling locations included in this study.Full size tableFungal endophytesTo assess fungal communities, a total of 352 samples from 145 native and non-native tree species, belonging to nine families of angiosperms and gymnosperms, were collected. Sampling was done at 44 locations in 28 countries on five continents (Fig. 1, Table 1).From each twig in a sample, one bud, one needle/leaf and one 1 cm long twig segment were taken (Fig. 1). Needles from gymnosperms, and leaves from evergreen angiosperms were sampled to accurately assess the risk of trading these species. Twig segments were cut from the twig bases. The selected plant parts were surface sterilized by immersion in 75% ethanol for 1 min, 4% NaOCl for 5 min, and 75% ethanol for 30 s26. After air drying on a sterile bench, the following material from each of 20 twigs per sample was pooled: half of one bud, a 0.5 cm long piece of a needle (from gymnosperms) or a 0.25 cm2 leaf (for evergreen angiosperms) and a 0.5 cm long piece of twig.DNA extraction, PCR amplification and Illumina sequencingTotal genomic DNA was extracted from 50 mg of pooled, surface sterilized, and ground tissue (Fig. 1) using DNeasy PowerPlant Pro Kit (Qiagen, Hilden, Germany), following the manufacturer’s instructions. For a total of 31 out of 352 samples, DNA was extracted from different tissues separately, and DNA extracts were then pooled. DNA concentrations were quantified using the Qubit dsDNA BR Assay Kit (Thermo Fisher Scientific, Waltham, USA) on a Qubit 3.0 Fluorometer (Thermo Fisher Scientific) and DNA was diluted to 5 ng/μl. Samples that yielded less than 5 ng/μl were not diluted. The ITS2 region was amplified with the 5.8S-Fung and ITS4-Fung primers27. PCR amplifications were carried out in 20 μl reaction volumes containing 25 ng of DNA template, 1 mg/ml BSA, 1 mM of MgCl2, 0.4 μM of each primer, and 0.76 × JumpStart REDTaq ReadyMix Reaction Mix (Sigma-Aldrich, Steinheim, Germany). PCR was performed using Veriti 96-Well Thermal Cycler (Applied Biosystems, Foster City, CA, USA) as described in Franić et al. (2019). Each sample was amplified in triplicates and successful PCR amplification confirmed by visualization of the PCR products, before and after pooling the triplicates, on 1.5% (w/v) agarose gel with ethidium bromide staining. Pooled amplicons were sent to the Génome Québec Innovation Center at McGill University (Montréal, Quebec, Canada) for barcoding using Fluidigm Access Array technology (Fluidigm, South San Francisco, CA, USA) and paired-end sequencing on the Illumina MiSeq v3 platform (Illumina Inc., San Diego, CA, USA). Raw sequences obtained in this study are deposited at the NCBI Sequence Read Archive under BioProject accession number PRJNA70814822.Bioinformatics and taxonomical classification of ASVsQuality filtering and delineation into ASVs were done with a customized pipeline28 largely based on VSEARCH29, as described by Herzog et al.30. The output data available on Figshare show the abundances of fungal ASVs in the samples24. Taxonomic classification of ASVs was conducted using Sintax31 implemented in VSEARCH against the UNITE v.7.2 database32 with a bootstrap support of 80%. The data on the taxonomic classification of fungal ASVs is deposited in Figshare24.Quality filtering, delineation into ASVs, and taxonomical assignments were done on a larger data set (total of 474 samples), which increased the confidence in the selected centroid sequences. This data set consisted of (1) sequences obtained from 352 samples of pooled tree tissues that are presented here22, (2) sequences obtained from 33 samples of pooled tree tissues which were not included in this manuscript due to violation of the common protocol, (3) sequences from 21 contaminated samples (positive DNA extraction controls), including sequences from the two control samples (not presented here), and (4) sequences obtained from 66 samples of non-pooled tree tissues of Pinus sylvestris and Quercus robur that were collected from the subset of locations considered in this study, but for a different study, and are thus not presented here.Herbivorous insectsInsects were assessed from 227 samples of 109 tree species, collected at 31 locations and in 18 countries (Fig. 1, Table 1).The collected twigs (twenty 50 cm twigs per species per location) were brought to a laboratory close to each sampling location and inspected for the presence of insects that overwinter as adults. Twigs were kept at room temperature with the cut ends immersed in water to induce budding and to allow the development of insects that overwinter as larvae, pupae or eggs. Twigs from each sample were protected with gauze bags to prevent insects moving between samples (Fig. 1). Twigs were inspected for the presence of insects daily for 4 weeks and all collected insects were stored in 95% ethanol for further examination.Morphological and molecular identificationInsects were inspected using a stereo microscope and sorted to taxonomic orders and feeding guilds (i.e. herbivores, predators, parasitoids and other). The abundance of the different feeding guilds and taxonomic orders in the samples is presented in a file deposited on Figshare24. Herbivorous insects were further sorted into morphospecies and at least one specimen per morphospecies was stored at −20 °C for molecular analysis. The abundance of the different morphospecies in each sample is presented in a file deposited on Figshare24. Specimens for molecular analysis were photographed with a Leica DVM6 digital microscope and the Leica Application Suite X (LAS X). Depending on the size of the insects, the whole individual or parts (e.g. legs, head) were used for molecular analysis. Genomic DNA was extracted with a KingFisher (Thermo Fisher Scientific) extraction protocol suitable for insects (35 min incubation at RT, 30 min wash at RT with 3 different washing buffers, 13 min elution at 60 °C) in a 96-well plate. PCR for the COI was carried out in 25 µl reaction volume with 2 µl diluted DNA (1:10), 0.5 µM of each of the primers LCO1490 and HCO219833 and 1 x REDTaq ReadyMix Reaction Mix (Sigma-Aldrich) using a Veriti 96-Well Thermal Cycler (Applied Biosystems) with the following setting: 2 min at 94 °C, five cycles of 30 s at 94 °C, 40 s at 45 °C, and 1 min at 72 °C, 35 cycles of 30 s at 94 °C, 50 s at 51 °C, and 1 min at 72 °C, and a final extension step at 72 °C for 10 min. The success of amplification was verified by electrophoresis of the PCR products in 1.5% (w/v) agarose gel at 90 V for 30 min with ethidium bromide staining. A standard Sanger sequencing of the PCR products in both directions with the same primers was done at Macrogen Europe, Amsterdam, Netherlands. Sequences were assembled and edited with CLC Workbench (Version 7.6.2, Quiagen) and compared to reference sequences in BOLD34. If no conclusive results were found, sequences were compared to reference sequences in the National Centre for Biotechnology Information (NCBI) GenBank databases35. Specimens were assigned to species if the query sequence showed less than 1% divergence from the reference sequence. If two or more taxa matched within the same range, the assignment was ranked down to the next taxonomic level (i.e., genus). When no species match was obtained based on the above criteria, a genus was assigned with a divergence of less than 3%. For lower taxonomic groups the 100 nearest sequences were inspected on the Blast Tree (Fast Minimum Evolution Method) and the taxonomic relationship was evaluated based on that tree. If none of the approaches above revealed a conclusive taxonomic assignment, the morphological identification was taken as reference. The results of morphological and molecular identification of insect specimens are presented in a file deposited on Figshare24. Insect sequences are deposited in GenBank database under accession numbers MW441337-MW44176725.Sample metadataPairwise geographic distances (Euclidean distances) between sampling locations were calculated based on the geographic coordinates of the locations, with function “dist” in the R statistical programme36.Climate data, including mean annual temperature, mean annual precipitation, and temperature seasonality were obtained from the WorldClim database37, at a resolution of 2.5 min, and represent averages between 1970 and 2000.A host-tree phylogeny was constructed with the phylomatic function from the package brranching38 in R using the “zanne2014” reference tree39. One Eucalyptus sample collected in Argentina and two Eucalyptus samples collected in Tunisia were not identified to species. To place them in the phylogeny, we assigned them to different congeneric species that were not sampled in this study and that we considered as representative samples of phylogenetic diversity from across Eucalyptus genus (E. viminalis, E. robusta and E. radiata). Pairwise phylogenetic distances between study tree species were calculated using the “cophenetic” function in R36.The described sample metadata are available in a file on Figshare24. More

Data collection: soil organic carbonThe process of data acquisition, selection and harmonisation is illustrated in the Supplementary Fig. S15 and in the Supplementary Tables S4–6. We conducted a systematic review for peer-reviewed journal articles, published before December 2018, from Web of Science, and Google Scholar with the search terms “(tree species OR forest) AND (soil organic carbon OR soil organic matter)”. We also used studies listed in two previously published meta-analyses16,17, or cited in already retained references (including references in English, French, Spanish, Portuguese, or Russian). For inclusion in the analysis we chose studies based on the following criteria: (1) the study reported soil organic carbon (SOC) or soil organic matter (SOM) concentrations or pools, at least in the topsoil layer and under at least two single-species forest stands; (2) the stands had to be older than 10 years81; (3) the stands had not experienced a major disturbance that differed between tree species, for at least 30 years (e.g., we rejected studies that compared natural forests with planted forests that were less than 30 years old); (4) The SOC concentration was More

Pure coordination gameIn this section we study the Pure Coordination Game (PCG) (also known as doorway game, or driving game) in which (R=1), (S=0), (T=0), and (P=1), resulting in a symmetric payoff matrix with respect to the two strategies:$$begin{gathered} begin{array}{*{20}c} {} & {quad ; {text{A}}} &; {text{B}} \ end{array}hfill \ begin{array}{*{20}c} {text{A}} \ {text{B}} \ end{array} left( {begin{array}{*{20}c} 1 & 0 \ 0 & 1 \ end{array} } right) hfill \ end{gathered}$$
(2)
There are two equivalent equilibria for both players coordinating at the strategy A or B (a third Nash equilibrium exists for players using a mix strategy of 50% A and 50% B). As the absolute values of the payoff matrix are irrelevant and the dynamics is defined by ratios between payoffs from different strategies, the payoff matrix (2) represents all games for which the relation (R=P >S=T) is fulfilled.In the PCG the dilemma of choosing between safety and benefit does not exist, because there is no distinction between risk-dominant and payoff-dominant equilibrium. Both strategies yield equal payoffs when players coordinate on them and both have the same punishment (no payoff) when players fail to coordinate. Therefore, the PCG is the simplest framework to test when coordination is possible and which factors influence it and how. It is in every player’s interest to use the same strategy as others. Two strategies, however, are present in the system at the beginning of the simulation in equal amounts. From the symmetry of the game we can expect no difference in frequency of each strategy being played, when averaged over many realisations. Still, the problem of when the system reaches full coordination in one of the strategies is not trivial. We address this question here.Figure 1Time evolution of the coordination rate (alpha) (in MC steps) in individual realisations for different values of the degree k in a random regular network of (N=1000) nodes, using (a) the replicator dynamics, (b) the best response, and (c) the unconditional imitation update rule.Full size imageFigure 2Coordination rate (alpha) and interface density (rho) vs degree k of a random regular network for (N=1000) using (a) the replicator dynamics, (b) the best response, and (c) the unconditional imitation update rule. Each green circle represents one of 500 realisations for each value of the degree k and the average value is plotted with a solid line, separately for (alpha >0.5) and (alpha le 0.5). Results are compared to the ER random network ((alpha _{ER})) with the same average degree.Full size imageFirst, we look at single trajectories as presented in Fig. 1. Some of them quickly reach (alpha =0) or 1, or stop in a frozen state without obtaining global coordination. Other trajectories take much longer and extend beyond the time scale showed in the figure. What we can already tell is that the process of reaching coordination is slower in the replicator dynamics where it usually takes more time than in the best response and unconditional imitation to reach a frozen configuration. For all update rules the qualitative effect of the connectivity is similar—for bigger degree it is more likely to obtain full coordination and it happens faster. For the UI, however, larger values of degree than for the RD and BR are required to observe coordination. For example, in the case of (k=10) or 20 the system stops in a frozen disorder when using UI, while for the RD and BR it quickly reaches a coordinated state of (alpha =0) or 1.To confirm the conclusions from observation of trajectories, we present the average outcome of the system’s evolution in the Fig. 2. The first thing to notice is that all plots are symmetrical with respect to the horizontal line of (alpha = 0.5). It indicates that the strategies are indeed equivalent as expected. In all cases there is a minimal connectivity required to obtain global coordination. For the RD and BR update rules this minimum value is (k=4), although in the case of BR the system fails to coordinate for small odd values of k due to regular character of the graph. This oscillating behaviour does not exist in Erdős–Rényi random networks. When nodes choose their strategies following the UI rule much larger values of k are required to obtain full coordination. Single realisations can result in (alpha = 0), or 1 already for (k=15). However, even for (k=60) there is still a possibility of reaching a frozen uncoordinated configuration.The important conclusion is that there is no coordination without a sufficient level of connectivity. In order to confirm that this is not a mere artefact of the random regular graphs we compare our results with those obtained for Erdős–Rényi (ER) random networks76,77 (black dashed line in Fig. 2). The level of coordination starts to increase earlier for the three update rules, but the general trend is the same. The only qualitative difference can be found in the BR. The oscillating level of coordination disappears and it doesn’t matter if the degree is odd or even. This shows that different behaviour for odd values of k is due to topological traps in random regular graphs78. Our results for the UI update rule are also consistent with previous work reporting coordination for a complete graph but failure of global coordination in sparse networks40.Figure 3Examples of frozen configuration reached under the UI update rule for small values of the average degree k in random regular networks (top row) and Erdős–Rényi networks (bottom row) with 150 nodes. Red colour indicates a player choosing the strategy A, blue colour the strategy B. Note the topological differences between random regular and ER networks when they are sparse. For (k=1) a random regular graph consists of pairs of connected nodes, while an ER network has some slightly larger components and many loose nodes. For (k=2) a random regular graph is a chain (sometimes 2–4 separate chains), while an ER network has one large component and many disconnected nodes. For (k=3) and (k=4) a random regular graph is always composed of one component, while an ER network has still a few disconnected nodes.Full size imageSince agents using the RD and BR update rule do not achieve coordination for small values of degree, one might suspect that the network is just not sufficiently connected for these values of the degree, i.e. there are separate components. This is only partially true. In Fig. 3, we can see the structures generated by random regular graph and by ER random graph algorithms. Indeed, for (k=1) and 2 the topology is trivial and a large (infinite for (k=1)) average path length23 can be the underlying feature stopping the system to reach coordination. For (k=3), however, the network is well connected with one giant component and the system still does not reach the global coordination when using RD or BR. For the UI update rule coordination arrives even for larger values of k. Looking at the strategies used by players in Fig. 3 we can see how frozen configuration without coordination can be achieved. There are various types of topological traps where nodes with different strategies are connected, but none of them is willing to change the strategy in the given update rule.We next consider the question of how the two strategies are distributed in the situations in which full coordination is not reached. Looking at the trajectories in Fig. 1 we can see that there are only few successful strategy updates in such scenario and the value of (alpha) remains close to 0.5 until arriving at a frozen state for (k=2) (also (k=7) for UI). This suggests that there is not enough time, in the sense of the number of updates, to cluster the different strategies in the network. Therefore, one might expect that they are well mixed as at the end of each simulation. However, an analysis of the density of active links in the final state of the dynamics, presented in Fig. 2, shows a slightly more complex behaviour. When the two strategies are randomly distributed (i.e. well mixed) in a network, the interface density takes the value (rho =0.5). When the two strategies are spatially clustered in the network there are only few links connecting them and therefore the interface density takes small values. Looking at the dependence of (rho) on k, we find that for the replicator dynamics the active link density starts at 0.5 for (k=1), then drops below 0.2 for (k=2) and 3 indicating good clustering between strategies, to fall to zero for (k=4) where full coordination is already obtained. When using the best response update rule the situation is quite different. For (k=1) there are no active links, (rho =0), and hardly any for (k=2). There is a slight increase of the active link density for (k=3), to drop to zero again for (k=4) due to full coordination. Because of the oscillatory level of coordination there are still active links for odd values of (kP) (otherwise we can rename the strategies and shuffle the columns and rows). What defines the outcome of a game are the greater than and smaller than relations among the payoffs. Therefore we can add/subtract any value from all payoffs, or multiply them by a factor grater than zero, without changing the game. Thus, the payoff matrix (1) can be rewritten as:$$begin{gathered} begin{array}{*{20}c} {} & {qquad {text{A}}} & {quad quad {text{B}}} \ end{array} ;; hfill \ begin{array}{*{20}c} {text{A}} \ {text{B}} \ end{array} left( {begin{array}{*{20}c} 1 & {frac{{S – P}}{{R – P}}} \ {frac{{T – P}}{{R – P}}} & 0 \ end{array} } right) hfill \ end{gathered}$$
(3)
which, after substituting (S’=frac{S-P}{R-P}) and (T’=frac{T-P}{R-P}), is equivalent to the matrix: $$begin{gathered} begin{array}{*{20}c} {} &quad ;;{text{A}} &; {text{B}} \ end{array} ;quad quad quad quad quad quad begin{array}{*{20}c} {} & quad; {text{A}} & ;{text{B}} \ end{array} hfill \ begin{array}{*{20}c} {text{A}} \ {text{B}} \ end{array} left( {begin{array}{*{20}c} 1 & {S^{prime}} \ {T^{prime}} & 0 \ end{array} } right)xrightarrow[{{text{apostrophes}}}]{{{text{skipping}}}}begin{array}{*{20}c} {text{A}} \ {text{B}} \ end{array} left( {begin{array}{*{20}c} 1 & S \ T & 0 \ end{array} } right) hfill \ end{gathered}$$
(4)
From now on we omit the apostrophes and simply refer to parameters S and T. This payoff matrix can represent many games, including e.g. the prisoner’s dilemma14,46 (for (T >1) and (S More

Taylor, M. W., Radax, R., Steger, D. & Wagner, M. Sponge-associated microorganisms: Evolution, ecology, and biotechnological potential. Microbiol. Mol. Biol. Rev. 71, 295–347 (2007).CAS 
PubMed 
PubMed Central 

Google Scholar 
Thomas, T. et al. Diversity, structure and convergent evolution of the global sponge microbiome. Nat. Commun. 7, 11870 (2016).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Webster, N. S. et al. Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ. Microbiol. 12, 2070–2082 (2010).CAS 
PubMed 
PubMed Central 

Google Scholar 
Sipkema, D. et al. Similar sponge-associated bacteria can be acquired via both vertical and horizontal transmission: Microbial transmission in Petrosia ficiformis. Environ. Microbiol. 17, 3807–3821 (2015).CAS 
PubMed 

Google Scholar 
Cleary, D. F. R. et al. The sponge microbiome within the greater coral reef microbial metacommunity. Nat. Commun. 10, 1644 (2019).Björk, J. R., Díez-Vives, C., Astudillo-García, C., Archie, E. A. & Montoya, J. M. Vertical transmission of sponge microbiota is inconsistent and unfaithful. Nat. Ecol. Evol. 3, 1172–1183 (2019).PubMed 
PubMed Central 

Google Scholar 
Webster, N. S. & Taylor, M. W. Marine sponges and their microbial symbionts: Love and other relationships. Environ. Microbiol. 14, 335–346 (2012).CAS 
PubMed 

Google Scholar 
Kennedy, J. et al. Evidence of a putative deep sea specific microbiome in marine sponges. PLoS ONE 9, e91092 (2014).ADS 
PubMed 
PubMed Central 

Google Scholar 
Steinert, G. et al. Compositional and quantitative insights into bacterial and archaeal communities of south pacific deep-sea sponges (Demospongiae and Hexactinellida). Front. Microbiol. 11, 716 (2020).Busch, K. et al. On giant shoulders: How a seamount affects the microbial community composition of seawater and sponges. Biogeosciences 17, 3471–3486 (2020).ADS 
CAS 

Google Scholar 
Olson, J. B. & Gao, X. Characterizing the bacterial associates of three Caribbean sponges along a gradient from shallow to mesophotic depths. FEMS Microbiol. Ecol. 85, 74–84 (2013).PubMed 

Google Scholar 
Steinert, G. et al. In four shallow and mesophotic tropical reef sponges from Guam the microbial community largely depends on host identity. PeerJ 4, e1936 (2016).PubMed 
PubMed Central 

Google Scholar 
Morrow, K. M., Fiore, C. L. & Lesser, M. P. Environmental drivers of microbial community shifts in the giant barrel sponge, Xestospongia muta, over a shallow to mesophotic depth gradient. Environ. Microbiol. 18, 2025–2038 (2016).CAS 
PubMed 

Google Scholar 
Ebada, S. S. & Proksch, P. The chemistry of marine sponges. In Handbook of Marine Natural Products (eds Fattorusso, E. et al.) 191–293 (Springer, 2012). https://doi.org/10.1007/978-90-481-3834-0_4.Chapter 

Google Scholar 
Kornprobst, J.-M. Porifera (Sponges). Encyclopedia of Marine Natural Products (Wiley, 2014).
Google Scholar 
Leal, M. C., Puga, J., Serôdio, J., Gomes, N. C. M. & Calado, R. Trends in the discovery of new marine natural products from invertebrates over the last two decades—Where and what are we bioprospecting?. PLoS ONE 7, e30580 (2012).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Blunt, J. W., Copp, B. R., Keyzers, R. A., Munro, M. H. G. & Prinsep, M. R. Marine natural products. Nat. Prod. Rep. 34, 235–294 (2017).CAS 
PubMed 

Google Scholar 
Unson, M. D., Holland, N. D. & Faulkner, D. J. A brominated secondary metabolite synthesized by the cyanobacterial symbiont of a marine sponge and accumulation of the crystalline metabolite in the sponge tissue. Mar. Biol. 119, 1–11 (1994).CAS 

Google Scholar 
Bewley, C. A., Holland, N. D. & Faulkner, D. J. Two classes of metabolites from Theonella swinhoei are localized in distinct populations of bacterial symbionts. Experientia 52, 716–722 (1996).CAS 
PubMed 

Google Scholar 
Wilson, M. C. et al. An environmental bacterial taxon with a large and distinct metabolic repertoire. Nature 506, 58–62 (2014).ADS 
CAS 
PubMed 

Google Scholar 
Tianero, M. D., Balaich, J. N. & Donia, M. S. Localized production of defence chemicals by intracellular symbionts of Haliclona sponges. Nat. Microbiol. 4, 1149–1159 (2019).CAS 
PubMed 

Google Scholar 
Ivanišević, J., Thomas, O. P., Lejeusne, C., Chevaldonné, P. & Pérez, T. Metabolic fingerprinting as an indicator of biodiversity: Towards understanding inter-specific relationships among Homoscleromorpha sponges. Metabolomics 7, 289–304 (2011).
Google Scholar 
Pérez, T. et al. Oscarella balibaloi, a new sponge species (Homoscleromorpha: Plakinidae) from the Western Mediterranean Sea: Cytological description, reproductive cycle and ecology: O. balibaloi: Description, reproductive cycle and ecology. Mar. Ecol. (Berl.) 32, 174–187 (2011).ADS 

Google Scholar 
Reveillaud, J. et al. Relevance of an integrative approach for taxonomic revision in sponge taxa: Case study of the shallow-water Atlanto-Mediterranean Hexadella species (Porifera: Ianthellidae: Verongida). Invertebr. Syst. 26, 230–248 (2012).
Google Scholar 
Olsen, E. K. et al. Marine AChE inhibitors isolated from Geodia barretti: Natural compounds and their synthetic analogs. Org. Biomol. Chem. 14, 1629–1640 (2016).CAS 
PubMed 

Google Scholar 
Reverter, M., Perez, T., Ereskovsky, A. V. & Banaigs, B. Secondary metabolome variability and inducible chemical defenses in the Mediterranean Sponge Aplysina cavernicola. J. Chem. Ecol. 42, 60–70 (2016).CAS 
PubMed 

Google Scholar 
Reverter, M., Tribalat, M.-A., Pérez, T. & Thomas, O. P. Metabolome variability for two Mediterranean sponge species of the genus Haliclona: Specificity, time, and space. Metabolomics 14, 114 (2018).Villegas-Plazas, M. et al. Variations in microbial diversity and metabolite profiles of the tropical marine sponge Xestospongia muta with season and depth. Microb. Ecol. 78, 243–256 (2019).CAS 
PubMed 

Google Scholar 
Mohanty, I. et al. Multi-omic profiling of Melophlus sponges reveals diverse metabolomic and microbiome architectures that are non-overlapping with ecological neighbors. Mar. Drugs 18, 124 (2020).CAS 
PubMed Central 

Google Scholar 
Bowerbank, J. S. On the anatomy and physiology of the Spongiadae. Part I. On the spicula. Philos. Trans. R. Soc. Lond. 148, 279–332 (1858).ADS 

Google Scholar 
Vosmaer, G. C. J. The sponges of the ‘Willem Barents’ expedition 1880 and 1881. Bijdragen tot de Dierkunde 12, 1–47 (1885).
Google Scholar 
Radax, R. et al. Metatranscriptomics of the marine sponge Geodia barretti: Tackling phylogeny and function of its microbial community. Environ. Microbiol. 14, 1308–1324 (2012).CAS 
PubMed 

Google Scholar 
Topsent, E. Spongiaires provenant des campagnes scientifiques de la ‘Princesse Alice’ dans les Mers du Nord (1898–1899—1906–1907). Résultats des campagnes scientifiques accomplies par le Prince Albert I. Monaco 45, 1–67 (1913).
Google Scholar 
Yashayaev, I. & Loder, J. W. Further intensification of deep convection in the Labrador Sea in 2016. Geophys. Res. Lett. 44, 1429–1438 (2017).ADS 

Google Scholar 
Gutleben, J. et al. Diversity of tryptophan halogenases in sponges of the genus Aplysina. FEMS Microbiol. Ecol. 95, fiz108 (2019).CAS 
PubMed 
PubMed Central 

Google Scholar 
Indraningrat, A. et al. Cultivation of sponge-associated bacteria from Agelas sventres and Xestospongia muta collected from different depths. Mar. Drugs 17, 578 (2019).CAS 
PubMed Central 

Google Scholar 
Ramiro-Garcia, J. et al. NG-Tax, a highly accurate and validated pipeline for analysis of 16S rRNA amplicons from complex biomes. F1000 Res. 5, 1791 (2018).
Google Scholar 
Yilmaz, P. et al. The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks. Nucl. Acids Res. 42, D643–D648 (2014).CAS 
PubMed 

Google Scholar 
Erngren, I., Smit, E., Pettersson, C., Cárdenas, P. & Hedeland, M. The effects of sampling and storage conditions on the metabolite profile of the marine sponge Geodia barretti. Front. Chem. 9:662659 (2021)Smith, C. A., Want, E. J., O’Maille, G., Abagyan, R. & Siuzdak, G. XCMS: Processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal. Chem. 78, 779–787 (2006).CAS 
PubMed 

Google Scholar 
Kuhl, C., Tautenhahn, R., Böttcher, C., Larson, T. R. & Neumann, S. CAMERA: An integrated strategy for compound spectra extraction and annotation of liquid chromatography/mass spectrometry data sets. Anal. Chem. 84, 283–289 (2012).CAS 
PubMed 

Google Scholar 
Oksanen, J. et al. vegan: Community Ecology Package (2017).Dat, T. T. H., Steinert, G., Thi Kim Cuc, N., Smidt, H. & Sipkema, D. Archaeal and bacterial diversity and community composition from 18 phylogenetically divergent sponge species in Vietnam. PeerJ 6, e4970 (2018).PubMed 
PubMed Central 

Google Scholar 
Miller, M. A., Pfeiffer, W. & Schwartz, T. Creating the CIPRES science gateway for inference of large phylogenetic trees. In 2010 Gateway Computing Environments Workshop (GCE) 1–8 (IEEE, 2010). https://doi.org/10.1109/GCE.2010.5676129.Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL) v4: Recent updates and new developments. Nucl. Acids Res. 47, W256–W259 (2019).CAS 
PubMed 
PubMed Central 

Google Scholar 
Thévenot, E. A., Roux, A., Xu, Y., Ezan, E. & Junot, C. Analysis of the human adult urinary metabolome variations with age, body mass index, and gender by implementing a comprehensive workflow for univariate and OPLS statistical analyses. J. Proteome Res. 14, 3322–3335 (2015).PubMed 

Google Scholar 
Weiss, S. et al. Correlation detection strategies in microbial data sets vary widely in sensitivity and precision. ISME J. 10, 1669–1681 (2016).CAS 
PubMed 
PubMed Central 

Google Scholar 
Deng, Y. et al. Molecular ecological network analyses. BMC Bioinform. 13, 113 (2012).
Google Scholar 
Friedman, J. & Alm, E. J. Inferring correlation networks from genomic survey data. PLoS Comput. Biol. 8, e1002687 (2012).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Durno, W. E., Hanson, N. W., Konwar, K. M. & Hallam, S. J. Expanding the boundaries of local similarity analysis. BMC Genom. 14, S3 (2013).
Google Scholar 
Reshef, D. N. et al. Detecting novel associations in large data sets. Science 334, 1518–1524 (2011).ADS 
CAS 
PubMed 
PubMed Central 
MATH 

Google Scholar 
Hall, M. M., Torres, D. J. & Yashayaev, I. Absolute velocity along the AR7W section in the Labrador Sea. Deep Sea Res. Part 1 Oceanogr. Res. Pap. 72, 72–87 (2013).
Google Scholar 
Reveillaud, J. et al. Host-specificity among abundant and rare taxa in the sponge microbiome. ISME J. 8, 1198–1209 (2014).CAS 
PubMed 
PubMed Central 

Google Scholar 
Moitinho-Silva, L. et al. Predicting the HMA-LMA status in marine sponges by machine learning. Front. Microbiol. 8, 752 (2017).Lidgren, G., Bohlin, L. & Bergman, J. Studies of Swedish marine organisms VII. A novel biologically active indole alkaloid from the sponge Geodia barretti. Tetrahedron Lett. 27, 3283–3284 (1986).CAS 

Google Scholar 
Sjögren, M. et al. Antifouling activity of brominated cyclopeptides from the marine sponge Geodia barretti. J. Nat. Prod. 67, 368–372 (2004).PubMed 

Google Scholar 
Sölter, S. Identifizierung und Synthese von Naturstoffen aus Borealen Schwämmen (Universität Hamburg, 2004).
Google Scholar 
Di, X. et al. 6-Bromoindole derivatives from the Icelandic marine sponge Geodia barretti: Isolation and anti-inflammatory activity. Mar. Drugs 16, 437 (2018).CAS 
PubMed Central 

Google Scholar 
Carstens, B. B. et al. Isolation, characterization, and synthesis of the barrettides: Disulfide-containing peptides from the marine sponge Geodia barretti. J. Nat. Prod. 78, 1886–1893 (2015).CAS 
PubMed 

Google Scholar 
Hedner, E. et al. Brominated cyclodipeptides from the marine sponge Geodia barretti as selective 5-HT ligands. J. Nat. Prod. 69, 1421–1424 (2006).CAS 
PubMed 

Google Scholar 
Hedner, E. et al. Antifouling activity of a dibrominated cyclopeptide from the marine sponge Geodia barretti. J. Nat. Prod. 71, 330–333 (2008).CAS 
PubMed 

Google Scholar 
Erwin, P. M., Pita, L., López-Legentil, S. & Turon, X. Stability of sponge-associated bacteria over large seasonal shifts in temperature and irradiance. Appl. Environ. Microbiol. 78, 7358–7368 (2012).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Cárdenas, C. A., Bell, J. J., Davy, S. K., Hoggard, M. & Taylor, M. W. Influence of environmental variation on symbiotic bacterial communities of two temperate sponges. FEMS Microbiol. Ecol. 88, 516–527 (2014).PubMed 

Google Scholar 
Glasl, B., Smith, C. E., Bourne, D. G. & Webster, N. S. Exploring the diversity-stability paradigm using sponge microbial communities. Sci. Rep. 8, 8425 (2018).Schöttner, S. et al. Relationships between host phylogeny, host type and bacterial community diversity in cold-water coral reef sponges. PLoS ONE 8, e55505 (2013).ADS 
PubMed 
PubMed Central 

Google Scholar 
Lurgi, M., Thomas, T., Wemheuer, B., Webster, N. S. & Montoya, J. M. Modularity and predicted functions of the global sponge-microbiome network. Nat. Commun. 10, 992 (2019).ADS 
PubMed 
PubMed Central 

Google Scholar 
Luter, H. M. et al. Microbiome analysis of a disease affecting the deep-sea sponge Geodia barretti. FEMS Microbiol. Ecol. 93, fix074 (2017).Thistle, D. Ecosystems of the Deep Oceans (Elsevier, 2003).
Google Scholar 
Pita, L., Erwin, P. M., Turon, X. & López-Legentil, S. Till death do us part: Stable sponge-bacteria associations under thermal and food shortage stresses. PLoS ONE 8, e80307 (2013).ADS 
PubMed 
PubMed Central 

Google Scholar 
Webster, N. S., Cobb, R. E. & Negri, A. P. Temperature thresholds for bacterial symbiosis with a sponge. ISME J. 2, 830–842 (2008).CAS 
PubMed 

Google Scholar 
Gerringer, M. E., Drazen, J. C. & Yancey, P. H. Metabolic enzyme activities of abyssal and hadal fishes: Pressure effects and a re-evaluation of depth-related changes. Deep Sea Res. Part 1 Oceanogr. Res. Pap. 125, 135–146 (2017).CAS 

Google Scholar 
Yashayaev, I. Hydrographic changes in the Labrador Sea, 1960–2005. Prog. Oceanogr. 73, 242–276 (2007).ADS 

Google Scholar 
Rhein, M., Steinfeldt, R., Kieke, D., Stendardo, I. & Yashayaev, I. Ventilation variability of Labrador Sea Water and its impact on oxygen and anthropogenic carbon: A review. Philos. Trans. A Math. Phys. Eng. Sci. 375, 20160321 (2017).ADS 
PubMed 
PubMed Central 

Google Scholar 
Galand, P. E., Potvin, M., Casamayor, E. O. & Lovejoy, C. Hydrography shapes bacterial biogeography of the deep Arctic Ocean. ISME J. 4, 564–576 (2010).PubMed 

Google Scholar 
Frank, A. H., Garcia, J. A. L., Herndl, G. J. & Reinthaler, T. Connectivity between surface and deep waters determines prokaryotic diversity in the North Atlantic Deep Water: North Atlantic dark ocean prokaryotic biogeography. Environ. Microbiol. 18, 2052–2063 (2016).PubMed 
PubMed Central 

Google Scholar 
Agogué, H., Lamy, D., Neal, P. R., Sogin, M. L. & Herndl, G. J. Water mass-specificity of bacterial communities in the North Atlantic revealed by massively parallel sequencing. Mol. Ecol. 20, 258–274 (2011).PubMed 

Google Scholar 
Djurhuus, A., Boersch-Supan, P. H., Mikalsen, S.-O. & Rogers, A. D. Microbe biogeography tracks water masses in a dynamic oceanic frontal system. R. Soc. Open Sci. 4, 170033 (2017).ADS 
PubMed 
PubMed Central 

Google Scholar 
Müller, O. et al. Spatiotemporal dynamics of ammonia-oxidizing Thaumarchaeota in distinct Arctic water masses. Front. Microbiol. 9, 1–13 (2018).ADS 

Google Scholar 
Kraemer, S., Ramachandran, A., Colatriano, D., Lovejoy, C. & Walsh, D. A. Diversity and biogeography of SAR11 bacteria from the Arctic Ocean. ISME J. https://doi.org/10.1038/s41396-019-0499-4 (2019).Article 
PubMed 
PubMed Central 

Google Scholar 
Monier, A. et al. Upper Arctic Ocean water masses harbor distinct communities of heterotrophic flagellates. Biogeosciences 10, 4273–4286 (2013).ADS 

Google Scholar 
Monier, A. et al. Oceanographic structure drives the assembly processes of microbial eukaryotic communities. ISME J. 9, 990–1002 (2015).CAS 
PubMed 

Google Scholar 
Corrège, T. The relationship between water masses and benthic ostracod assemblages in the western Coral Sea, Southwest Pacific. Palaeogeogr. Palaeoclimatol. Palaeoecol. 105, 245–266 (1993).
Google Scholar 
Muhling, B. A., Beckley, L. E., Koslow, J. A. & Pearce, A. F. Larval fish assemblages and water mass structure off the oligotrophic south-western Australian coast: SW Australian larval fish assemblages. Fish. Oceanogr. 17, 16–31 (2007).
Google Scholar 
Eerkes-Medrano, D. et al. A community assessment of the demersal fish and benthic invertebrates of the Rosemary Bank Seamount Marine Protected Area (NE Atlantic). Deep Sea Res. Part 1 Oceanogr. Res. Pap. https://doi.org/10.1016/j.dsr.2019.103180 (2019).Article 

Google Scholar 
Puerta, P. et al. Influence of water masses on the biodiversity and biogeography of deep-sea benthic ecosystems in the North Atlantic. Front. Mar. Sci. 7, 239 (2020).Roberts, E. et al. Water masses constrain the distribution of deep-sea sponges in the North Atlantic Ocean and Nordic Seas. Mar. Ecol. Prog. Ser. 659, 75–96 (2021).ADS 

Google Scholar 
Kenchington, E. et al. Connectivity modelling of areas closed to protect vulnerable marine ecosystems in the northwest Atlantic. Deep Sea Res. Part 1 Oceanogr. Res. Pap. 143, 85–103 (2019).
Google Scholar 
Louca, S. et al. Function and functional redundancy in microbial systems. Nat. Ecol. Evol. 2, 936–943 (2018).PubMed 

Google Scholar 
McCauley, M., Chiarello, M., Atkinson, C. L. & Jackson, C. R. Gut microbiomes of freshwater mussels (Unionidae) are taxonomically and phylogenetically variable across years but remain functionally stable. Microorganisms 9, 411 (2021).CAS 
PubMed 
PubMed Central 

Google Scholar 
Page, M., West, L., Northcote, P., Battershill, C. & Kelly, M. Spatial and temporal variability of cytotoxic metabolites in populations of the New Zealand Sponge Mycale hentscheli. J. Chem. Ecol. 31, 1161–1174 (2005).CAS 
PubMed 

Google Scholar 
Ternon, E., Perino, E., Manconi, R., Pronzato, R. & Thomas, O. P. How environmental factors affect the production of guanidine alkaloids by the Mediterranean sponge Crambe crambe. Mar. Drugs 15, 181 (2017).PubMed Central 

Google Scholar 
Sacristán-Soriano, O., Banaigs, B. & Becerro, M. A. Temporal trends in the secondary metabolite production of the sponge Aplysina aerophoba. Mar. Drugs 10, 677–693 (2012).PubMed 
PubMed Central 

Google Scholar 
Ivanisevic, J. et al. Biochemical trade-offs: Evidence for ecologically linked secondary metabolism of the sponge Oscarella balibaloi. PLoS ONE 6, e28059 (2011).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Burg, M. B. & Ferraris, J. D. Intracellular organic osmolytes: Function and regulation. J. Biol. Chem. 283, 7309–7313 (2008).CAS 
PubMed 
PubMed Central 

Google Scholar 
Nau-Wagner, G., Boch, J., Le Good, J. A. & Bremer, E. High-affinity transport of choline-O-sulfate and its use as a compatible solute in Bacillus subtilis. Appl. Environ. Microbiol. 65, 560–568 (1999).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Popowich, A., Zhang, Q. & Le, X. C. Arsenobetaine: The ongoing mystery. Natl. Sci. Rev. 3, 451–458 (2016).CAS 

Google Scholar 
Connor, K. M. & Gracey, A. Y. High-resolution analysis of metabolic cycles in the intertidal mussel Mytilus californianus. Am. J. Physiol. Regul. Integr. Comp. Physiol. 302, R103–R111 (2012).CAS 
PubMed 

Google Scholar 
Cárdenas, P. Who produces Ianthelline? The Arctic sponge Stryphnus fortis or its sponge Epibiont Hexadella dedritifera: A probable case of sponge–sponge contamination. J. Chem. Ecol. 42, 339–347 (2016).PubMed 

Google Scholar 
Steffen, K. et al. Barrettides: A peptide family specifically produced by the deep-sea sponge Geodia barretti. J. Nat. Prod. 84, 3138–3146 (2021).CAS 
PubMed 
PubMed Central 

Google Scholar 
Abbamondi, G. R., De Rosa, S., Iodice, C. & Tommonaro, G. Cyclic dipeptides produced by marine sponge-associated bacteria as quorum sensing signals. Nat. Prod. Commun. 9, 229–232 (2014).CAS 
PubMed 

Google Scholar 
Kasheverov, I. et al. 6-Bromohypaphorine from Marine Nudibranch Mollusk Hermissenda crassicornis is an agonist of human α7 nicotinic acetylcholine receptor. Mar. Drugs 13, 1255–1266 (2015).CAS 
PubMed 
PubMed Central 

Google Scholar 
Moitinho-Silva, L. et al. The sponge microbiome project. Gigascience 6, 1–7 (2017).CAS 
PubMed 

Google Scholar 
Kielak, A. M., Barreto, C. C., Kowalchuk, G. A., van Veen, J. A. & Kuramae, E. E. The ecology of acidobacteria: Moving beyond genes and genomes. Front. Microbiol. 7, 744 (2016).Crits-Christoph, A., Diamond, S., Butterfield, C. N., Thomas, B. C. & Banfield, J. F. Novel soil bacteria possess diverse genes for secondary metabolite biosynthesis. Nature 558, 440–444 (2018).ADS 
CAS 
PubMed 

Google Scholar  More

To our knowledge, this study provides the first recorded information on the active swimming of Japanese eels and on their transport by currents in the open ocean. Specifically, the strong flow of the KC largely dominated the movements of the eels and transported them northeastward while they swam mainly southward, and active swimming contributed a little to their travel trajectories. In contrast, the swimming of eels made a relatively higher contribution to their travel trajectories in the TS area.Our in situ estimates of the mean swimming speeds of Japanese eels (26–41 cm/s) were similar or slightly lower than those of European eels. In the acoustic tracking experiment of European eels considering environmental current vectors, their swimming speeds were 35–58 cm/s in the coastal midwater26. In a laboratory experiment using stamina tunnels with stable temperatures, the optimal swimming speeds of European eels were estimated to be 61–68 cm/s (0.74–1.02 BL/s)56, which were higher than the in situ estimates. The minimum swimming speed of European eels is considered to be 40 cm/s if they will arrive at their spawning area in the Sargasso Sea (distance of 5500 km) in 6 months, and their optimal swimming speeds were sufficient to migrate over the long distance in time for the near-spawning period after escape from their growth habitats56. However, field studies using PSAT tagging also reported that in situ migration speeds (including transport by currents) were less than the optimal swimming speeds and suggested that some European eels could reach their spawning area within the near-spawning periods and that others only arrive in time for the following spawning season19.Our estimated effective swimming speed of Japanese eels, all day and all night over the tracking periods, ranged from 3 to 30 cm/s with individual variations. These estimates were consistent with the swimming speeds (excluding transport by currents) of 2.2–15.1 km/day (2–18 cm/s) estimated in the PSAT study of Japanese eels14. Silver-phase Japanese eels start migrating from their coastal growth habitats in Japan primarily in October to December57, 58, and spawning near the West Mariana Ridge occurs in April to August33, 35. Numerical models assuming that migrating eels use true navigation (readjusted compass) or a constant compass heading (fixed compass from the departure place to the spawning site) indicate that the minimal swimming speed required to arrive at the spawning area within 8 months is 10–12 cm/s37. Our estimated effective swimming speeds of five out of ten eels during the day and eight out of ten eels during the night were similar or higher than these minimal speeds. The low effective swimming speeds frequently observed during the day might be due to the relatively low values observed in the swimming speed at 10 min intervals and the swimming directions often varying during the day. When eels swim with stable orientation, as observed in three of the eels (WE2999_TS, WE3001_TS, and WE3002_TS) during the night, the effective swimming speeds exceeded 25 cm/s. If such a stable orientation is maintained and compensate the low speeds during the day, the eels that leave during autumn and winter will be able to arrive at the spawning area during the next spring to summer.It should also be noted that the swimming speeds in body length per second were significantly higher in shallow water during the night than in deep water during the day. In the open ocean, anguillid species exhibit DVMs during oceanic migration, swimming at depth during the day and in the shallows during the night9,10,11,12,13,14,15,16,17,18,19,20,21,22. These DVMs are likely related to the possible avoidance from visual predators under light conditions19 or maturation control59. Essentially, through the DVMs, the eels encounter low temperatures ( 20 °C) during the same day. Generally, the swimming speeds of fishes are restricted by the ambient water temperature60, and the water temperature encountered through DVMs might influence the horizontal-swimming speeds of Japanese eels.Other factors besides swimming speed are important for the success of eel migrations, such as adapting to mesopelagic zones that silver eels undergo during their spawning migrations. The most important and obvious morphological adaptation in mesopelagic fish is their well-developed eyes, and migrating eels also seem to use this strategy. These fish often have relatively large pupils61, high photosensitive structures, such as tubular eyes62, a pure rod multibank retina63, and maximum rhodopsin absorption to adapt to the blue-green light in the deep sea64. The eyes of catadromous eels displayed enlargement during their transformation into migrating silver-phase eels65, 66 and potentially increase their retinal surface area, which results in the possibility of increased photon capture. In addition, the rhodopsins in the eyes change from a freshwater type with a maximum absorption of ~ 500 nm to a deep-sea type with a maximum absorption of ~ 480 nm67,68,69. Their extreme sensitivity to light is evident through their DVM in mesopelagic water, where the timing of a large descent and ascent in the DVM demonstrated by migrating catadromous eels is precisely synchronized with sunrise and sunset. Furthermore, eels alter their swimming depth in response to the phase of the Moon9, 15, 20, 21, appearing to be capable of perceiving extremely low-intensity moonlight.This study showed that three eels released in the TS area (mainly 300–400-m depth) and one eel in the KC area (near surface) were found to change their swimming direction around the time of the solar culmination when the Sun’s bearing changed. The clockwise and counterclockwise trajectories of these eels corresponded to whether the Sun moved from the east to west in the southern and northern sky, suggesting that they demonstrated horizontal negative phototaxis swimming to avoid sunlight. They might move to avoid high-intensity sunlight horizontally, not vertically, as they gradually increase the swimming depths possibly due to acclimation to cold deep water after release. The daytime swimming depths of the eels became deeper day-by-day after their release (Fig. 4); a similar phenomenon was observed in European eels12, American eels17, and long fin eels13. Recently, Higuchi et al.20 observed that the daytime swimming depths of Japanese eels released in the TS area gradually became deeper until 13 days after their release. These facts indicate that they gradually acclimate to the cold water at the deep depths after release. Since this tracking study was conducted 2–8 days after their release, the daytime swimming depth of eels would not have reached a steady state yet. The relatively high intensity from sunlight at the shallow depths where eels swam immediately after release in the TS area might cause horizontal avoidance behavior from the light.In other cases, many eels, especially those released in the KC area, did not demonstrate the rotational behavior. The eels in the KC area mostly stayed deeper (500–800 m) during the day than the eels in the TS area (stayed at depths of 300–600 m) even during the periods shortly after their release. This is possibly due to higher water temperatures even at the deeper depths in the KC area (Fig. 4). The eels in the TS area did not demonstrate clear rotational behavior at depths of more than 400 m. The PSAT studies have reported that the steady swimming depths during the day were 500–800 m14, 20. Therefore, it was assumed that the rotational behavior observed in some eels was not a regular behavior during their migration. However, the rotational behavior observed in this study suggests that they surely perceive the horizontal direction of Sun’s bearing at 400 m depths at least. Generally, they exhibit DVM precisely synchronizing with sunrise and sunset and surely perceive the change in sunlight intensity at deeper depths9,10,11,12,13,14,15,16,17,18,19,20,21,22. Even though the rotational behavior were not observed below 400 m, it remains unknown whether the eels could not perceive the Sun’s bearing from the light penetrated at depth; thus, further investigation of response to underwater light is required in future.While possible negative phototaxis behaviors were observed in some eels after release around the time of solar culmination, the trajectories of ten eels during the entire period of tracking experiments implied that each eel tended to swim meridionally toward the bearing of the Sun at culmination. We observed that eels released at middle (20°–34° N) and low (12°–13°N) latitudes tended to swim southward and northward in the meridional direction, respectively (Fig. 6A, B). The tendency to move in a north–south swimming direction corresponded to whether the Sun culminated to the north or south: eels swam southward if the culmination occurred in the southern sky, but they swam northward if it occurred in the northern sky (Fig. 6). In the KC area (33°–35° N), the Sun rose in the southeast, passed celestial meridian in the southern sky, and set in the southwest (Fig. 6C). At 20° N in the summer time when the tracking study was conducted, the Sun also passed a celestial meridian in the southern sky, but rose in the northeast and set in the northwest (Fig. 6C). When Sun culmination occurred in the southern sky, the meridional swimming directions tended to be southward (Fig. 6A). However, at 12° to 13° N in the summer time, the Sun rose in the northeast, passed the celestial meridian in the northern sky, and set in the northwest (Fig. 6D). When the Sun at culmination appeared in the northern sky, the meridional swimming directions tended to be northward (Fig. 6B). Furthermore, the swimming behavior by one eel (WE4264_TS) that was released slightly south (14° 15′ N) from the latitude with the Sun passing through the zenith was also indicative of the meridional swimming traits. This eel moved in a northerly direction on the first day, but then it lost its north–south bias in swimming around 14° 30′ N, where the Sun nearly passed through the zenith (Figs. 1 and 6D). These observations imply that the eels might move toward the latitude with the Sun passing through the zenith.Figure 6Swimming trajectories of eels and solar paths in the celestial sphere viewed from east during each tracking period. Swimming trajectories of eels released at (A) 20°N in the tropical–subtropical area and the Kuroshio Current area, and (B) 12°–14°15′N in the tropical–subtropical area. Solar paths through the north (N)–south (S) axis and the zenith at the time of tracking in (C) 20°N in the tropical–subtropical area and the Kuroshio Current area, and (D) 12°–14°15′N in the tropical–subtropical area.Full size imageTheoretically, it is possible for mesopelagic animals to use solar cues for navigation at depths shallower than the asymptotic depth, below which penetrating light rays are symmetrical around the vertical axis and the polarization plane becomes horizontal. For example, the Sargasso Sea, where the two Atlantic catadromous eels spawn1, 3, has extremely transparent water70, and the major axis of radiance distribution still remains tilted in the mesopelagic zone. The angle of maximum radiance of sunlight at 475 nm was 13° at depths of 400 m when the Sun’s elevation was 60° (Fig. 7)52, 53. In highly transparent water, the asymptotic depth could be as high as 1000–1200 m, and the depths below this cannot be utilized for compass use53. Currently, it is not possible to verify whether the Sun culminating to north or south caused the meridional swimming tendencies of eels in this study. Potentially, these meridional swimming tendencies could be due to other orientation clues, such as the geomagnetic field, as discussed for temperate anguillid eels17, 45. Nevertheless, in future studies, it would be worthwhile considering solar cues as a possible candidate factor in the orientation of eels, even when under faint underwater light conditions.Figure 7Optical features of underwater sunlight. (A) Schematic diagram of sunlight penetrating the deep ocean at 90° to the solar bearing. The line of arrows indicates the major axis of the incident beam in a vertical plane perpendicular to the Sun’s bearing. Blue light (around 475 nm) reaches the lowest depths. With increasing depth, the light field alters its character into a less directed distribution and a lower energetic level through scattering and absorption processes. Penetrating light rays are symmetrical around the region below the asymptotic depth. (B) An example of spectral radiance distribution (e. g. 475 nm) at a certain depth. The radiance distribution is shown by an ellipsoid and the major axis is drawn by a line with arrow. The refracted angular deviation (a) of the major axis of underwater radiance distribution from the vertical axis equals the tilt of the electric vector (ee bar) from the horizontal axis53. When the Sun’ s elevation was 60° in the Sargasso Sea, the radiance distributions were measured at three different depths and the tilt of the electric vector were estimated to be 24° at depths of 100 m and 200 m and 13° at depth of 400 m52, 53.Full size imageGiven that eels might be able to use the Sun’s bearing at culmination to orient their meridional swimming direction, this orientation scheme could support a clockwise eel migration route following a partial subtropical gyre2, 37. Japanese eels that departed from the nursery area first transported northeastward via the strong KC. Maintaining southward swimming in the current, they eventually crossed the current and shifted to the southward migration course. When they enter the KC, movement to the left of the bearing of the Sun at culmination (i.e., south) is the typical pattern for the early migration of eels from Japan. The movements of eels observed in the KC were consistent with the expected route; however, eels released at low latitudes of the TS area often swam northward but also westward, which resulted in their traveling an unreasonable distance from the spawning area. This might be due to their behavior during early migration. In this study, eels were transported from Japan and released into the open ocean at low latitudes. They might have swum toward the expected bearing of the Sun at culmination as if they were in the north and moved to the left of the Sun’s bearing along with the North Equatorial Current, which would mimic the early migration of eels leaving Japan and moving along the KC.Among the eels tracked in this study were individuals with impaired swim bladders, yellow-phase eels in the process of hormone-treatment maturation, and silver-phase eels collected from different rivers in different years. Despite these variations, the swimming characteristics of the eels did not differ in terms of their DVM behavior16 and swimming speed. Nevertheless, confirmation of our results using samples with a uniform status in future research would be highly desirable. In this study, the tracked eel position was assumed to be identical to that of the tracking ship and the errors between these two positions could not be evaluated; thus, the positioning of tracked fish also may need to be improved in future studies. Experimental studies, such as tracking of blind, magnetically disturbed, or olfactory-blocked eels, could help obtain or eliminate alternative candidate clues and enhance our understanding of the navigational system of anguillid eels. Controlled laboratory experiments are required to directly quantify the ability of eels to perceive radiance distribution or polarization, along with any associated behaviors. In addition, the internal clock of eels required to perform celestial navigation should be investigated. Meanwhile, the results obtained from this study can enhance our knowledge of the mechanisms underlying the migratory behaviors of eels in the open ocean. More