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    Nitrogen and carbon stable isotope analysis sheds light on trophic competition between two syntopic land iguana species from Galápagos

    Luiselli, L., Akani, G. & Capizzi, D. Food resource partitioning of a community of snakes in a swamp rainforest of south-eastern Nigeria. J. Zool. 246(2), 125–133. https://doi.org/10.1111/j.1469-7998.1998.tb00141.x (1998).Article 

    Google Scholar 
    Rouag, R., Djilali, H., Gueraiche, H. & Luiselli, L. Resource partitioning patterns between two sympatric lizard species from Algeria. J. Arid Environ. 69, 158–168. https://doi.org/10.1016/j.jaridenv.2006.08.008 (2007).ADS 
    Article 

    Google Scholar 
    Bergeron, R. & Blouin-Demers, G. Niche partitioning between two sympatric lizards in the Chiricahua Mountains of Arizona. Copeia 108(3), 570–577. https://doi.org/10.1643/CH-19-268 (2020).Article 

    Google Scholar 
    Lucek, K., Butlin, R. K. & Patsiou, T. Secondary contact zones of closely-related Erebia butterflies overlap with narrow phenotypic and parasitic clines. J. Evol. Biol. 33(9), 1152–1163. https://doi.org/10.1111/jeb.13669 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Freeman, B. G. Competitive interaction upon secondary contact drive elevational divergence in tropical birds. Am. Nat. 186(4), 470–479. https://doi.org/10.5061/dryad.6qg3g (2015).Article 
    PubMed 

    Google Scholar 
    Schoener, T. W. Resource partitioning in ecological communities. Science 185(4145), 27–39 (1974).ADS 
    CAS 
    Article 

    Google Scholar 
    Rivas, L. R. A Reinterpretation of the concepts “sympatric” and “allopatric” with proposal of the additional terms “syntopic” and “allotopic”. Syst. Zool. 13(1), 42 (1964).Article 

    Google Scholar 
    Macarthur, R. & Levins, R. The limiting similarity, convergence, and divergence of coexisting species. Am. Nat. 101(921), 377–385 (1967).Article 

    Google Scholar 
    Dayan, T. & Simberloff, D. Ecological and community-wide character displacement: The next generation. Ecol. Lett. 8(8), 875–894. https://doi.org/10.1111/j.1461-0248.2005.00791.x (2005).Article 

    Google Scholar 
    Holomuzki, J. R., Feminella, J. W. & Power, M. E. Biotic interactions in freshwater benthic habitats. J. N. Am. Benthol. Soc. 29(1), 220–244. https://doi.org/10.1899/08-044.1 (2010).Article 

    Google Scholar 
    Ferretti, F. et al. Competition between wild herbivores: Reintroduced red deer and Apennine chamois. Behav. Ecol. 26(2), 550–559. https://doi.org/10.1093/beheco/aru226 (2015).Article 

    Google Scholar 
    Takada, H., Yano, R., Katsumata, A., Takatsuki, S. & Minami, M. Diet compositions of two sympatric ungulates, the Japanese serow (Capricornis crispus) and the sika deer (Cervus nippon), in a montane forest and an alpine grassland of Mt. Asama central, Japan. Mamm. Biol. 101, 681–694. https://doi.org/10.1007/s42991-021-00122-5 (2021).Article 

    Google Scholar 
    Hubbel, S. P. The Unified Neutral Theory of Biodiversity and Biogeography (Princeton University Press, 2001) (ISBN 9780691021287).
    Google Scholar 
    Bell, G. Neutral macroecology. Science 293, 2413–2418. https://doi.org/10.1126/science.293.5539.2413 (2001).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Rosindell, J., Hubbel, S. P. & Etienne, R. S. The unified neutral theory of biodiversity and biogeography at age ten. Trends Ecol. Evol. 26(7), 340–348. https://doi.org/10.1016/j.tree.2011.03.024 (2011).Article 
    PubMed 

    Google Scholar 
    Cowie, R. H. & Holland, B. S. Dispersal is fundamental to biogeography and the evolution of biodiversity on oceanic islands. J. Biogeogr. 33, 193–198. https://doi.org/10.1111/j.1365-2699.2005.01383.x (2006).Article 

    Google Scholar 
    Amarasekare, P. & Nisbet, R. M. Spatial heterogeneity, source-sink dynamics, and the local coexistence of competing species. Am. Nat. 158(6), 572–584. https://doi.org/10.1086/323586 (2001).CAS 
    Article 
    PubMed 

    Google Scholar 
    Kumar, K., Gentile, G. & Grant, T. D. Conolophus subcristatus. The IUCN Red List of Threatened Species 2020, e.T5240A3014082 (2020). https://doi.org/10.2305/IUCN.UK.2020-2.RLTS.T5240A3014082.enGentile, G. Conolophus marthae. The IUCN Red List of Threatened Species 2012, e. T174472A1414375 (2012). https://doi.org/10.2305/IUCN.UK.2012-1.RLTS.T174472A1414375.enGentile, G., Marquez, C., Snell, H. L., Tapia, W. & Izurieta, A. Conservation of a New Flagship Species: The Galápagos Pink Land Iguana (Conolophus marthae Gentile and Snell, 2009). In Problematic Wildlife: A Cross-Disciplinary Approach (ed. Angelici, F. M.) 315–336 (Springer International Publishing, 2016). https://doi.org/10.1007/978-3-319-22246-2_15.Chapter 

    Google Scholar 
    Gentile, G. & Snell, H. L. Conolophus marthae sp. Nov. (Squamata, iguanidae), a new species of land iguana from the Galápagos Archipelago. Zootaxa 2201, 1–10 (2009).Article 

    Google Scholar 
    Colosimo, G. et al. Chemical signatures of femoral pore secretions in two syntopic but reproductively isolated species of Galápagos land iguanas (Conolophus marthae and C. subcristatus). Sci. Rep. 10(1), 14314. https://doi.org/10.1038/s41598-020-71176-7 (2020).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Jackson, M. Galápagos: A Natural History, Revised and Expanded (University of Calgary Press, 1994).
    Google Scholar 
    Traveset, A. et al. Galápagos land iguana (Conolophus subcristatus) as a seed disperser. Integr. Zool. 11(3), 207–213. https://doi.org/10.1111/1749-4877.12187 (2016).Article 
    PubMed 

    Google Scholar 
    Di Giambattista, L. et al. Molecular data exclude current hybridization between iguanas Conolophus marthae and C. subcristatus on Wolf volcano (Galápagos islands). Conserv. Genet. 19(6), 1461–1469. https://doi.org/10.1007/s10592-018-1114-3 (2018).Article 

    Google Scholar 
    MacLeod, A. et al. Hybridization masks speciation in the evolutionary history of the Galápagos marine iguana. Proc. R. Soc. B 282, 1–9. https://doi.org/10.1098/rspb.2015.0425 (2015).Article 

    Google Scholar 
    Gause, G. F. The Struggle for Existence (Williams and Wilkins Company, 1934).Book 

    Google Scholar 
    Hardin, G. The competitive exclusion principle. Science 131(3409), 1292–1297 (1960).ADS 
    CAS 
    Article 

    Google Scholar 
    Ashrafi, S., Beck, A., Rutishauser, M., Arlettaz, R. & Bontadina, F. Trophic niche partitioning of cryptic species of long-eared bats in Switzerland: Implications for conservation. Eur. J. Wildl. Res. 57, 843–849. https://doi.org/10.1007/s10344-011-0496-z (2011).Article 

    Google Scholar 
    Bleyhl, B. et al. Assessing niche overlap between domestic and threatened wild sheep to identify conservation priority areas. Divers. Distrib. 25(1), 129–141. https://doi.org/10.1111/ddi.12839 (2019).Article 

    Google Scholar 
    Newsome, S. D., del Rio, C. M., Bearhop, S. & Phillips, D. L. A niche for isotopic ecology. Front. Ecol. Environ. 5(8), 429–436. https://doi.org/10.1890/060150.1 (2007).Article 

    Google Scholar 
    Riera, P., Stal, L. J. & Nieuwenhuize, J. δ13C versus δ15N of co-occurring mollusks within a community dominated by Crassostrea gigas and Crepidula ornicate (Oossterschelde, The Netherlands). Mar. Ecol. Prog. Ser. 240, 291–295 (2002).ADS 
    Article 

    Google Scholar 
    Page, B., McKenzie, J. & Goldsworthy, S. D. Dietary resources partitioning among sympatric New Zealand and Australian fur seals. Mar. Ecol. Prog. Ser. 293, 283–302 (2005).ADS 
    Article 

    Google Scholar 
    DeNiro, M. J. & Epstein, S. Influence of diet on the distribution of carbon isotopes in animals. Geochim. Cosmochim. Acta 42(5), 495–506 (1978).ADS 
    CAS 
    Article 

    Google Scholar 
    DeNiro, M. J. & Epstein, S. Influence of diet on the distribution of nitrogen isotopes in animals. Geochim. Cosmochim. Acta 45(3), 341–351 (1981).ADS 
    CAS 
    Article 

    Google Scholar 
    Post, D. M. Using stable isotopes to estimate trophic position: Models, methods, and assumptions. Ecology 83(3), 703–718. https://doi.org/10.1890/0012-9658(2002)083[0703:USITET]2.0.CO;2 (2002).Article 

    Google Scholar 
    Crawford, K., McDonald, R. A. & Bearhop, S. Applications of stable isotope techniques to the ecology of mammals. Mammal. Rev. 38(1), 87–107. https://doi.org/10.1111/j.1365-2907.2008.00120.x (2008).Article 

    Google Scholar 
    Trueman, M. & d’Ozouville, N. Characterizing the Galápagos terrestrial climate in the face of global climate change. Gala Res. 67, 26–37 (2010).
    Google Scholar 
    Paltán, H. A. et al. Climate and sea surface trends in the Galápagos Islands. Sci. Rep. 11(1), 1–13. https://doi.org/10.1038/s41598-021-93870-w (2021).CAS 
    Article 

    Google Scholar 
    Rivas-Torres, G. F., Benítez, F. L., Rueda, D., Sevilla, C. & Mena, C. F. A methodology for mapping native and invasive vegetation coverage in archipelagos: An example from the Galápagos islands. Prog. Phys. Geogr. 42(1), 83–111. https://doi.org/10.1177/0309133317752278 (2018).Article 

    Google Scholar 
    Gentile, G., Ciambotta, M. & Tapia, W. Illegal wildlife trade in Galápagos: Molecular tools help taxonomic identification and guide rapid repatriation of confiscated iguanas. Conserv. Genet. Resour. 5, 867–872. https://doi.org/10.1007/s12686-013-9915-7 (2013).Article 

    Google Scholar 
    Stephens, R. B., Ouimette, A. P., Hobbie, E. A. & Rowe, R. J. Re-evaluating trophic discrimination factors (Δδ13C and Δδ15N) for diet reconstruction. Ecol. Mono 92, e1525. https://doi.org/10.1002/ecm.1525 (2022).CAS 
    Article 

    Google Scholar 
    Hobson, K. A. & Clark, R. G. Assessing avian diets using stable isotopes I: Turnover of 13C in tissues. The Condor 94(1), 181–188. https://doi.org/10.2307/1368807 (1992).Article 

    Google Scholar 
    Li, C.-H., Roth, J. D. & Detwiler, J. T. Isotopic turnover rates and diet-tissue discrimination depend on feeding habits of freshwater snails. PLoS ONE 13(7), e0199713. https://doi.org/10.1371/journal.pone.0199713 (2018).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Steinitz, R., Lemm, J., Pasachnik, S. & Kurle, C. Diet-tissue stable isotope (δ13C and δ15N) discrimination factors for multiple tissues from terrestrial reptiles. Rapid Commun. Mass Spectrom. 30(1), 9–21. https://doi.org/10.1002/rcm.7410 (2016).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Ethier, D. M., Kyle, C. J., Kyser, T. K. & Nocera, J. J. Variability in the growth patterns of the cornified claw sheath among vertebrates: Implications for using biogeochemistry to study animal movement. Can. J. Zool. 88(11), 1043–1051. https://doi.org/10.1139/Z10-073 (2010).Article 

    Google Scholar 
    Aresco, M. J. & James, F. C. Ecological relationships of turtles in northern Florida lakes: A study of omnivory and the structure of a lake food web. Florida Fish and Wildlife Conservation Commission (2005). https://www.semanticscholar.org/paper/ECOLOGICAL-RELATIONSHIPS-OF-TURTLES-IN-NORTHERN-A-A-Aresco-James/f6d59265eb6494aa19cfde7d2d80bb165e6432acLourenço, P. M., Granadeiro, J. P., Guilherme, J. L. & Catry, T. Turnover rates of stable isotopes in avian blood and toenails: Implications for dietary and migration studies. J. Exp. Mar. Biol. Ecol. 472, 89–96. https://doi.org/10.1016/j.jembe.2015.07.006 (2015).CAS 
    Article 

    Google Scholar 
    Jackson, A. L., Inger, R., Parnell, A. C. & Bearhop, S. Comparing isotopic niche widths among and within communities: SIBER—Stable isotope Bayesian ellipses in r. J. Animal Ecol. 80(3), 595–602. https://doi.org/10.1111/j.1365-2656.2011.01806.x (2011).Article 

    Google Scholar 
    Wikelski, M. & Romero, L. M. Body size, performance and fitness in Galápagos marine iguanas. Integr Comp Biol 43(3), 376–386. https://doi.org/10.1093/icb/43.3.376 (2003).Article 
    PubMed 

    Google Scholar 
    Iverson, J., Smith, G. & Pieper, L. Factors Affecting Long-Term Growth of the Allen Cays Rock Iguana in the Bahamas. In Iguanas: Biology and Conservation (eds Alberts, A. et al.) 176–192 (University of California Press, 2004). https://doi.org/10.1525/9780520930117-018.Chapter 

    Google Scholar 
    Smith, G. R. & Iverson, J. B. Effects of tourism on body size, growth, condition, and demography in the Allen Cay Iguana. Herpetol. Conserv. Biol. 11, 214–221 (2016).
    Google Scholar 
    Wikelski, M., Carrillo, V. & Trillmich, F. Energy limits to body size in a grazing reptile, the Galápagos Marine Iguana. Ecology 78(7), 2204–2217. https://doi.org/10.2307/2265956 (1997).Article 

    Google Scholar 
    Bulakhova, N. A. et al. Inter-observer and intra-observer differences in measuring body length: A test in the common lizard, Zootoca vivipara. Amphibia-Reptilia 32(4), 477–484. https://doi.org/10.1163/156853811X601636 (2011).Article 

    Google Scholar 
    R Development Core Team. R: A language and environment for statistical computing (2021). https://cran.r-project.orgGoslee, S. C. & Urban, D. L. The ecodist package for dissimilarity-based analysis of ecological data. J. Stat. Softw. 22(7), 1–19. https://doi.org/10.18637/jss.v022.i07 (2007).Article 

    Google Scholar 
    Randin, C. F., Jaccard, H., Vittoz, P., Yoccoz, N. G. & Guisan, A. Land use improves spatial predictions of mountain plant abundance but not presence–absence. J. Veg. Sci. 20, 996–1008. https://doi.org/10.1111/j.1654-1103.2009.01098.x (2009).Article 

    Google Scholar 
    Broennimann, O., Di Cola, V. & Guisan, A. ecospat: Spatial Ecology Miscellaneous Methods. R package version 3.2.1 (2022) https://CRAN.R-project.org/package=ecospatBorcard, D., Legendre, P. & Drapeau, P. Partialling out the spatial component of ecological variation. Ecology 73(3), 1045–1055. https://doi.org/10.2307/1940179 (1992).Article 

    Google Scholar 
    Wood, S. N. Generalized Additive Models: An Introduction with R 2nd edn. (Chapman and Hall/CRC, 2017). https://doi.org/10.1201/9781315370279.Book 
    MATH 

    Google Scholar 
    Van Marken Lichtenbelt, W. D. Optimal foraging of a herbivorous lizard, the green iguana in a seasonal environment. Oecologia 95, 246–256. https://doi.org/10.1007/BF00323497 (1993).ADS 
    Article 
    PubMed 

    Google Scholar 
    Pasachnik, S. A. & Martin-Velez, V. An evaluation of the diet of Cyclura iguanas in the Dominican Republic. Herpetol. Bull. 140, 6–12 (2017).
    Google Scholar 
    Cerling, T. E. et al. Global vegetation change through the Miocene/Pliocene boundary. Nature 389(6647), 153–158. https://doi.org/10.1038/38229 (1997).ADS 
    CAS 
    Article 

    Google Scholar 
    O’Leary, M. H. Carbon isotopes in photosynthesis. Bioscience 38(5), 328–336. https://doi.org/10.2307/1310735 (1988).Article 

    Google Scholar 
    Snell, H. L. & Tracy, C. R. Behavioral and morphological adaptations by Galapagos land iguanas (Conolophus subcristatus) to water and energy requirements of eggs and neonates. Am. Zool. 25(4), 1009–1018. https://doi.org/10.1093/icb/25.4.1009 (1985).Article 

    Google Scholar 
    Christian, K., Tracy, C. R. & Porter, W. P. Diet, digestion, and food preferences of Galápagos land iguanas. Herpetologica 40(2), 205–212 (1984).
    Google Scholar 
    Mallona, I., Egea-Cortines, M. & Weiss, J. Conserved and divergent rhythms of crassulacean acid metabolism-related and core clock gene expression in the cactus Opuntia ficus-indica. Plant Physiol. 156, 1978–1989. https://doi.org/10.1104/pp.111.179275 (2011).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    San Sebastián, O., Navarro, J., Llorente, G. A. & Richter-Boix, Á. Trophic strategies of a non-native and a native amphibian species in shared ponds. PLoS ONE 10(6), 1–17. https://doi.org/10.1371/journal.pone.0130549 (2015).CAS 
    Article 

    Google Scholar 
    Perga, M. E. & Grey, J. Laboratory measures of isotope discrimination factors: Comments on Caut, Angulo & Courchamp (2008, 2009). J. Appl. Ecol. 47(4), 942–947. https://doi.org/10.1111/j.1365-2664.2009.01730.x (2010).CAS 
    Article 

    Google Scholar 
    Freeman, B. Sexual niche partitioning in two species of new Guinean Pachycephala whistlers. J. Field Ornithol. 85(1), 23–30. https://doi.org/10.1111/jofo.12046 (2014).Article 

    Google Scholar 
    Werner, D. I. Social Organization and Ecology of Land Iguanas, Conolophus subcristatus, on Isla Fernandina, Galápagos. In Iguanas of the World: Their Behavior, Ecology, and Conservation (eds Burghardt, G. M. & Rand, A. S.) 342–365 (Noyes Publications, 1982).
    Google Scholar 
    Doi, H., Akamatsu, F. & González, A. L. Starvation effects on nitrogen and carbon stable isotopes of animals: An insight from meta-analysis of fasting experiments. R. Soc. Open Sci. 4(8), 170633. https://doi.org/10.1098/rsos.170633 (2017).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Persaud, A., Dillon, P., Molot, L. & Hargan, K. Relationships between body size and trophic position of consumers in temperate freshwater lakes. Aquat. Sci. 74(1), 203–212. https://doi.org/10.1007/s00027-011-0212-9 (2012).Article 

    Google Scholar 
    Keppeler, F. W. et al. Body size, trophic position, and the coupling of different energy pathways across a saltmarsh landscape. Limnol. Oceanogr. Lett. 6(6), 360–368. https://doi.org/10.1002/lol2.10212 (2021).Article 

    Google Scholar 
    Hanson, J. O. et al. Feeding across the food web: The interaction between diet, movement and body size in estuarine crocodiles (Crocodylus porosus). Austral. Ecol. 40(3), 275–286. https://doi.org/10.1111/aec.12212 (2015).Article 

    Google Scholar 
    Gustavino, B., Terrinoni, S., Paglierani, C. & Gentile, G. Conolophus marthae vs. Conolophus subcristatus: Does the skin pigmentation pattern exert a protective role against DNA damaging effect induced by UV light exposure? Analysis of blood smears through the micronucleus test. Paper presented at the Galápagos Land and Marine Iguanas Workshop, IUCN SSC Iguana Specialist Group Meeting, Puerto Ayora, 28–29 October 2014.Di Giacomo, C. et al. 25–Hydroxivitamin D plasma levels in natural populations of pigmented and partially pigmented land iguanas from Galápagos (Conolophus spp.). Hind 2022, 1–9. https://doi.org/10.1155/2022/7741397 (2022).CAS 
    Article 

    Google Scholar 
    Percie du Sert, N. et al. Reporting animal research: Explanation and elaboration for the ARRIVE guidelines 2.0. PLoS Biol. 18(7), e3000411. https://doi.org/10.1371/journal.pbio.3000411 (2020).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar  More

  • in

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

    Google Scholar  More

  • in

    Ornaments are equally informative in male and female birds

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

  • in

    The pulsating soft coral Xenia umbellata shows high resistance to warming when nitrate concentrations are low

    Doney, S. C. et al. Climate change impacts on marine ecosystems. Annu. Rev. Mar. Sci. 4, 11–37. https://doi.org/10.1146/annurev-marine-041911-111611 (2012).ADS 
    Article 

    Google Scholar 
    Hoegh-Guldberg, O., Poloczanska, E. S., Skirving, W. & Dove, S. Coral reef ecosystems under climate change and ocean acidification. Front. Mar. Sci. 4, 158 (2017).Article 

    Google Scholar 
    Weis, V. M. Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. J. Exp. Biol. 211, 3059–3066 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    Fitt, W., Brown, B., Warner, M. & Dunne, R. Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20, 51–65. https://doi.org/10.1007/s003380100146 (2001).Article 

    Google Scholar 
    Fujise, L., Yamashita, H., Suzuki, G. & Koike, K. Expulsion of zooxanthellae (Symbiodinium) from several species of scleractinian corals: comparison under non-stress conditions and thermal stress conditions. Galaxea, JCRS 15, 29–36. https://doi.org/10.3755/galaxea.15.29 (2013).Article 

    Google Scholar 
    Rädecker, N. et al. Heat stress destabilizes symbiotic nutrient cycling in corals. PNAS USA https://doi.org/10.1073/pnas.2022653118 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    LaJeunesse, T. C. et al. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. 28, 2570-2580.e6. https://doi.org/10.1016/j.cub.2018.07.008 (2018).CAS 
    Article 
    PubMed 

    Google Scholar 
    Wooldridge, S. A. Breakdown of the coral-algae symbiosis. Towards formalising a linkage between warm-water bleaching thresholds and the growth rate of the intracellular zooxanthellae. Biogeosciences 10, 1647–1658 (2013).ADS 
    Article 

    Google Scholar 
    Wiedenmann, J. et al. Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nat. Clim. Change 3, 160–164 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    Peña-García, D., Ladwig, N., Turki, A. J. & Mudarris, M. S. Input and dispersion of nutrients from the Jeddah Metropolitan Area, Red Sea. Mar. Pollut. Bull. 80, 41–51. https://doi.org/10.1016/j.marpolbul.2014.01.052 (2014).CAS 
    Article 
    PubMed 

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

    Google Scholar 
    Ferrier-Pagés, C., Gattuso, J.-P., Dallot, S. & Jaubert, J. Effect of nutrient enrichment on growth and photosynthesis of the zooxanthellate coral Stylophora pistillata. Coral Reefs 19, 103–113. https://doi.org/10.1007/s003380000078 (2000).Article 

    Google Scholar 
    Rosset, S., Wiedenmann, J., Reed, A. J. & D’angelo, C. Phosphate deficiency promotes coral bleaching and is reflected by the ultrastructure of symbiotic dinoflagellates. Mar. Pollut. Bull. 118, 180–187. https://doi.org/10.1016/j.marpolbul.2017.02.044 (2017).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Patterson, K. et al. Distinct signalling pathways and transcriptome response signatures differentiate ammonium- and nitrate-supplied plants. Plant Cell Environ. 33, 1486–1501 (2010).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ezzat, L., Maguer, J.-F., Grover, R. & Ferrier-Pagès, C. New insights into carbon acquisition and exchanges within the coral–dinoflagellate symbiosis under NH 4+ and NO 3− supply. Proc. R. Soc. B. 282, 20150610 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Guan, Y., Hohn, S., Wild, C. & Merico, A. Vulnerability of global coral reef habitat suitability to ocean warming, acidification and eutrophication. Glob. Change Biol. 26, 5646–5660 (2020).ADS 
    Article 

    Google Scholar 
    Roff, G. & Mumby, P. J. Global disparity in the resilience of coral reefs. Trends Ecol. Evol. 27, 404–413 (2012).PubMed 
    Article 

    Google Scholar 
    Knowlton, N. & Jackson, J. B. C. Shifting baselines, local impacts, and global change on coral reefs. PLoS Biol. 6, e54 (2008).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Vollstedt, S., Xiang, N., Simancas-Giraldo, S. M. & Wild, C. Organic eutrophication increases resistance of the pulsating soft coral Xenia umbellata to warming. PeerJ 8, e9182 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Fabricius, K. E., Cséke, S., Humphrey, C. & De’ath, G. Does trophic status enhance or reduce the thermal tolerance of scleractinian corals? A review, experiment and conceptual framework. PloS one 8, e54399 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Cardini, U. et al. Functional significance of dinitrogen fixation in sustaining coral productivity under oligotrophic conditions. Proc. Biol. Sci. 282, 20152257 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    Baker, D. M., Freeman, C. J., Wong, J. C. Y., Fogel, M. L. & Knowlton, N. Climate change promotes parasitism in a coral symbiosis. ISME J. 12, 921–930. https://doi.org/10.1038/s41396-018-0046-8 (2018).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    de Barros, F. et al. Unravelling the different causes of nitrate and ammonium effects on coral bleaching. Sci. Rep. 10, 11975 (2020).ADS 
    Article 

    Google Scholar 
    Steinberg, R. K., Dafforn, K. A., Ainsworth, T. & Johnston, E. L. Know thy anemone. A review of threats to octocorals and anemones and opportunities for their restoration. Front. Mar. Sci. 7, 590 (2020).Article 

    Google Scholar 
    Norström, A. V., Nyström, M., Lokrantz, J. & Folke, C. Alternative states on coral reefs. Beyond coral–macroalgal phase shifts. Mar. Ecol. Prog. Ser. 376, 295–306 (2009).ADS 
    Article 

    Google Scholar 
    van de Water, J. A. J. M., Allemand, D. & Ferrier-Pagès, C. Host-microbe interactions in octocoral holobionts—recent advances and perspectives. Microbiome 6, 64 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Syms, C. & Jones, G. P. Dysturbance, habitat structure, and the dynamics of a coral-reef fish community. Ecology 81, 2714–2729 (2000).Article 

    Google Scholar 
    Syms, C. & Jones, G. P. Soft corals exert no direct effects on coral reef fish assemblages. Oecologia 127, 560–571. https://doi.org/10.1007/s004420000617 (2001).ADS 
    Article 
    PubMed 

    Google Scholar 
    Epstein, H. E. & Kingsford, M. J. Are soft coral habitats unfavourable? A closer look at the association between reef fishes and their habitat. Environ. Biol. Fishes 102, 479–497 (2019).Article 

    Google Scholar 
    Janes, M. P. Distribution and diversity of the soft coral family Xeniidae (Coelenterata: Octocorallia) in Lembeh Strait, Indonesia. Galaxea, JCRS 15, 195–200 (2013).Article 

    Google Scholar 
    Fox, H. E., Pet, J. S., Dahuri, R. & Caldwell, R. L. Recovery in rubble fields. Long-term impacts of blast fishing. Mar. Pollut. Bull. 46, 1024–1031 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    Al-Sofyani, A. A. & Niaz, G. R. A comparative study of the components of the hard coral Seriatopora hystrix and the soft coral Xenia umbellata along the Jeddah coast, Saudi Arabia. Rev. Biol. Mar. Oceanogr. 42, 207–219 (2007).Article 

    Google Scholar 
    Kremien, M., Shavit, U., Mass, T. & Genin, A. Benefit of pulsation in soft corals. PNAS USA 110, 8978–8983 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Swart, P. K., Saied, A. & Lamb, K. Temporal and spatial variation in the δ 15 N and δ 13 C of coral tissue and zooxanthellae in Montastraea faveolata collected from the Florida reef tract. Limnol. Oceanogr. 50, 1049–1058 (2005).ADS 
    CAS 
    Article 

    Google Scholar 
    Grottoli, A. G., Tchernov, D. & Winters, G. Physiological and biogeochemical responses of super-corals to thermal stress from the northern gulf of Aqaba, Red Sea. Front. Mar. Sci. 4, 215 (2017).Article 

    Google Scholar 
    Tanaka, Y., Miyajima, T., Koike, I., Hayashibara, T. & Ogawa, H. Imbalanced coral growth between organic tissue and carbonate skeleton caused by nutrient enrichment. Limnol. Oceanogr. 52, 1139–1146 (2007).ADS 
    CAS 
    Article 

    Google Scholar 
    Marubini, F. & Davies, P. S. Nitrate increases zooxanthellae population density and reduces skeletogenesis in corals. Mar. Biol. 127, 319–328 (1996).CAS 
    Article 

    Google Scholar 
    Dagenais-Bellefeuille, S. & Morse, D. Putting the N in dinoflagellates. Front. Microbiol. https://doi.org/10.3389/fmicb.2013.00369 (2013).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wooldridge, S. A. A new conceptual model for the warm-water breakdown of the coral—algae endosymbiosis. Mar. Freshwater Res. 60, 483 (2009).CAS 
    Article 

    Google Scholar 
    Moed, J. R. & Hallegraeff, G. M. Some problems in the estimation of chlorophyll-a and phaeopigments from pre- and post-acidification spectrophotometrie measurements. Int. Revue Ges. Hydrobiol. Hydrogr. 63, 787–800 (1978).CAS 
    Article 

    Google Scholar 
    Redfield, A. C. The biological control of chemical factors in the environment. Am. Sci. 46, A221-230A (1958).
    Google Scholar 
    Pupier, C. A., Bednarz, V. N. & Ferrier-Pagès, C. Studies with soft corals—recommendations on sample processing and normalization metrics. Front. Mar. Sci. 5, 2620 (2018).Article 

    Google Scholar 
    Pupier, C. A. et al. Dissolved nitrogen acquisition in the symbioses of soft and hard corals with Symbiodiniaceae: A key to understanding their different nutritional strategies?. Front. Microbiol. 12, 657759 (2021).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bednarz, V. N., Naumann, M. S., Niggl, W. & Wild, C. Inorganic nutrient availability affects organic matter fluxes and metabolic activity in the soft coral genus Xenia. J. Exp. Biol. 215, 3672–3679 (2012).CAS 
    PubMed 

    Google Scholar 
    Béraud, E., Gevaert, F., Rottier, C. & Ferrier-Pagès, C. The response of the scleractinian coral Turbinaria reniformis to thermal stress depends on the nitrogen status of the coral holobiont. J. Exp. Biol. 216, 2665–2674 (2013).PubMed 

    Google Scholar 
    Ezzat, L., Towle, E., Irisson, J.-O., Langdon, C. & Ferrier-Pagès, C. The relationship between heterotrophic feeding and inorganic nutrient availability in the scleractinian coral T. reniformis under a short-term temperature increase. Limnol. Oceanogr. 61, 89–102 (2016).ADS 
    Article 

    Google Scholar 
    Dobson, K. L. et al. Moderate nutrient concentrations are not detrimental to corals under future ocean conditions. Mar. Biol. https://doi.org/10.1007/s00227-021-03901-3 (2021).Article 

    Google Scholar 
    Strychar, K. B., Coates, M., Sammarco, P. W., Piva, T. J. & Scott, P. T. Loss of Symbiodinium from bleached soft corals Sarcophyton ehrenbergi, Sinularia sp. and Xenia sp.. J. Exp. Mar. Biol. Ecol. 320, 159–177. https://doi.org/10.1016/j.jembe.2004.12.039 (2005).Article 

    Google Scholar 
    Sammarco, P. W. & Strychar, K. B. Responses to high seawater temperatures in zooxanthellate octocorals. PloS one 8, e54989 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Osman, E. O. et al. Thermal refugia against coral bleaching throughout the northern Red Sea. Glob. Change Biol. 24, e474–e484. https://doi.org/10.1111/gcb.13895 (2018).Article 

    Google Scholar 
    Fine, M., Gildor, H. & Genin, A. A coral reef refuge in the Red Sea. Glob. Change Biol. 19, 3640–3647 (2013).ADS 
    Article 

    Google Scholar 
    Evensen, N. R., Fine, M., Perna, G., Voolstra, C. R. & Barshis, D. J. Remarkably high and consistent tolerance of a Red Sea coral to acute and chronic thermal stress exposures. Limnol. Oceanogr. 66, 1718–1729 (2021).ADS 
    Article 

    Google Scholar 
    Sawall, Y. et al. Extensive phenotypic plasticity of a Red Sea coral over a strong latitudinal temperature gradient suggests limited acclimatization potential to warming. Sci. Rep. 5, 8940 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Carpenter, E. J., Harvey, H., Fry, B. & Capone, D. G. Biogeochemical tracers of the marine cyanobacterium Trichodesmium. Deep-Sea Res. I: Oceanogr. Res. Pap. 44, 27–38 (1997).ADS 
    CAS 
    Article 

    Google Scholar 
    Kürten, B. et al. Influence of environmental gradients on C and N stable isotope ratios in coral reef biota of the Red Sea, Saudi Arabia. J. Sea Res. 85, 379–394 (2014).ADS 
    Article 

    Google Scholar 
    Karcher, D. B. et al. Nitrogen eutrophication particularly promotes turf algae in coral reefs of the central Red Sea. PeerJ 8, e8737 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Sterner, R. W. & Elser, J. J. Ecological Stoichiometry. The Biology of Elements from Molecules to the Biosphere (Princeton University Press, 2002).Tilstra, A. et al. Light induced intraspecific variability in response to thermal stress in the hard coral Stylophora pistillata. PeerJ 5, e3802 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Siebeck, U. E., Marshall, N. J., Klüter, A. & Hoegh-Guldberg, O. Monitoring coral bleaching using a colour reference card. Coral Reefs 25, 453–460 (2006).ADS 
    Article 

    Google Scholar 
    Venn, A. A., Wilson, M. A., Trapido-Rosenthal, H. G., Keely, B. J. & Douglas, A. E. The impact of coral bleaching on the pigment profile of the symbiotic alga, Symbiodinium. Plant Cell Environ. 29, 2133–2142 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    Dubinsky, Z. V. Y. et al. The effect of external nutrient resources on the optical properties and photosynthetic efficiency of Stylophora pistillata. Proc. R. Soc. B.: Biol. Sci. 239, 231–246 (1990).ADS 

    Google Scholar 
    Fabricius, K. E. Effects of irradiance, flow, and colony pigmentation on the temperature microenvironment around corals: Implications for coral bleaching?. Limnol. Oceanogr. 51, 30–37 (2006).ADS 
    Article 

    Google Scholar 
    Nordemar, I., Nyström, M. & Dizon, R. Effects of elevated seawater temperature and nitrate enrichment on the branching coral Porites cylindrica in the absence of particulate food. Mar. Biol. 142, 669–677 (2003).CAS 
    Article 

    Google Scholar 
    Lewis, J. B. Feeding behaviour and feeding ecology of the Octocorallia (Coelenterata: Anthozoa). J. Zool. 196, 371–384 (1982).Article 

    Google Scholar 
    Studivan, M. S., Hatch, W. I. & Mitchelmore, C. L. Responses of the soft coral Xenia elongata following acute exposure to a chemical dispersant. SpringerPlus 4, 80 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Parrin, A. P. et al. Symbiodinium migration mitigates bleaching in three octocoral species. J. Exp. Mar. Biol. Ecol. 474, 73–80 (2016).Article 

    Google Scholar 
    Parrin, A. P. et al. Within-colony migration of symbionts during bleaching of octocorals. Biol. Bull. 223, 245–256 (2012).PubMed 
    Article 

    Google Scholar 
    Bourne, D. G., Morrow, K. M. & Webster, N. S. Insights into the coral microbiome. Underpinning the health and resilience of reef ecosystems. Annu. Rev. Microbiol. 70, 317–340 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Furnas, M., Mitchell, A., Skuza, M. & Brodie, J. In the other 90%: phytoplankton responses to enhanced nutrient availability in the Great Barrier Reef Lagoon. Mar. Pollut. Bull. 51, 253–265 (2005).CAS 
    PubMed 
    Article 

    Google Scholar 
    Ziegler, M. et al. Coral microbial community dynamics in response to anthropogenic impacts near a major city in the central Red Sea. Mar. Pollut. Bull. https://doi.org/10.1016/j.marpolbul.2015.12.045 (2016).Article 
    PubMed 

    Google Scholar 
    Gruber, R. et al. Marine monitoring program: Annual report for inshore water quality monitoring 2018–19. Report for the Great Barrier Reef Marine Park Authority. GBRMPA, Townsville (2020).Dinesen, Z. D. Patterns in the distribution of soft corals across the central Great Barrier Reef. Coral Reefs 1, 229–236. https://doi.org/10.1007/BF00304420 (1983).ADS 
    Article 

    Google Scholar 
    Benayahu, Y. et al. Octocorals of the Indo-Pacific. In Mesophotic Coral Ecosystems Vol. 12 (eds Loya, Y. et al.) 709–728 (Springer International Publishing, Cham, 2019).Chapter 

    Google Scholar 
    Tilot, V., Leujak, W., Ormond, R. F. G., Ashworth, J. A. & Mabrouk, A. Monitoring of South Sinai coral reefs: Influence of natural and anthropogenic factors. Aquat. Conserv. 18, 1109–1126 (2008).Article 

    Google Scholar 
    D’Angelo, C. & Wiedenmann, J. Impacts of nutrient enrichment on coral reefs. New perspectives and implications for coastal management and reef survival. Curr. Opin. Environ. Sustain. 7, 82–93 (2014).Article 

    Google Scholar 
    Wooldridge, S. A. & Done, T. J. Improved water quality can ameliorate effects of climate change on corals. Ecol. Appl. 19, 1492–1499 (2009).PubMed 
    Article 

    Google Scholar 
    Nugues, M. M. & Roberts, C. M. Partial mortality in massive reef corals as an indicator of sediment stress on coral reefs. Mar. Pollut. Bull. 46, 314–323 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    LeGresley, M. & McDermott, G. Counting chamber methods for quantitative phytoplankton analysis – haemocytometer, Palmer-Maloney cell and Sedgewick-Rafter cell. In Microscopic and Molecular Methods for Quantitative Phytoplankton Analysis, edited by B. Karlson, C. Cusack & E. Bresnan (IOC UNESCO, Paris, France, 2010), pp. 25–30.Jeffrey, S. W. & Humphrey, G. F. New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem. Physiol. Pflanz. 167, 191–194 (1975).CAS 
    Article 

    Google Scholar 
    D’Angelo, C. et al. Blue light regulation of host pigment in reef-building corals. Mar. Ecol. Prog. Ser. 364, 97–106 (2008).ADS 
    Article 

    Google Scholar 
    Feys, J. Nonparametric tests for the interaction in two-way factorial designs using R. R J. 8, 367 (2016).Article 

    Google Scholar 
    Noguchi, K., Gel, Y. R., Brunner, E. & Konietschke, F. nparLD An R software package for the nonparametric analysis of longitudinal data in factorial experiments. J. Stat. Soft. 50, 1–23 (2012).Article 

    Google Scholar 
    Schlöder, C. & D’Croz, L. Responses of massive and branching coral species to the combined effects of water temperature and nitrate enrichment. J. Exp. Mar. Biol. Ecol. 313, 255–268 (2004).Article 

    Google Scholar 
    Faxneld, S., Jörgensen, T. L. & Tedengren, M. Effects of elevated water temperature, reduced salinity and nutrient enrichment on the metabolism of the coral Turbinaria mesenterina. Estuar. Coast. Shelf Sci. 88, 482–487 (2010).ADS 
    CAS 
    Article 

    Google Scholar 
    Chumun, P. K. et al. High nitrate levels exacerbate thermal photo-physiological stress of zooxanthellae in the reef-building coral Pocillopora damicornis. Eco-Eng. 25, 1–9 (2013).
    Google Scholar 
    Higuchi, T., Yuyama, I. & Nakamura, T. The combined effects of nitrate with high temperature and high light intensity on coral bleaching and antioxidant enzyme activities. Reg. Stud. Mar. Sci. 2, 27–31 (2015).
    Google Scholar  More

  • in

    Ancient DNA provides insights into 4,000 years of resource economy across Greenland

    Raghavan, M. et al. The genetic prehistory of the New World Arctic. Science 345, 1255832 (2014).Meldgaard, M. Ancient Harp Seal Hunters of Disko Bay (Museum Tusculanum Press, 2004).Grønnow, B. & Jensen, J. F. The Northernmost Ruins of the Globe: Eigil Knuth’s Archaeological Investigations in Peary Land and Adjacent Areas of High Arctic Greenland (Museum Tusculanum Press, 2003).Jensen, J. F. in The Oxford Handbook of the Prehistoric Arctic (eds Friesen, T. M. & Mason, O.) 673–691 (Oxford Univ. Press, 2016). https://doi.org/10.1093/oxfordhb/9780199766956.013.56Buckland, P. C., Ski, A. M. A. Y. E. W., Mcgovern, T. H. & Ogilvie, A. E. J. Bioarchaeological and climatological evidence for the fate of Norse farmers in medieval Greenland. Antiquity 70, 88–96 (1996).Article 

    Google Scholar 
    Gulløv, H. C. Grønlands Forhistorie (Gyldendal, 2004).Friesen, T. M. & Arnold, C. D. The timing of the Thule migration: new dates from the Western Canadian. Soc. Am. Archaeol. 73, 527–538 (2008).
    Google Scholar 
    Moltke, I. et al. Uncovering the genetic history of the present-day Greenlandic population. Am. J. Hum. Genet. 96, 54–69 (2015).CAS 
    Article 

    Google Scholar 
    Gulløv, H. C. From Middle Ages to Colonial Times: Archaeological and Ethnohistorical Studies of the Thule Culture in South West Greenland 1300–1800 AD (Dansk Polar Center, 1997).Gulløv, H. C. et al. Danmark og Kolonierne: Grønland (Gads Forlag, 2017).Ameen, C. et al. Specialized sledge dogs accompanied Inuit dispersal across the North American Arctic. Proc. R. Soc. B 286, 20191929 (2019).Grønnow, B. et al. At the edge: High Arctic Walrus hunters during the Little Ice Age. Antiquity 85, 960–977 (2011).Article 

    Google Scholar 
    Fitzhugh, B. in The Oxford Handbook of the Prehistoric Arctic (eds Friesen, M. & Mason, O.) 253–278 (Oxford Univ. Press, 2016).Lyman, R. L. Vertebrate Taphonomy (Cambridge Univ. Press, 1994).Seersholm, F. V. et al. DNA evidence of bowhead whale exploitation by Greenlandic Paleo-Inuit 4000 years ago. Nat. Commun. 7, 13389 (2016). https://doi.org/10.1038/ncomms13389Betts, M. in The Oxford Handbook of the Prehistoric Arctic (eds Friesen, M. & Mason, O.) 81–108 (Oxford Univ. Press, 2016). https://doi.org/10.1093/oxfordhb/9780199766956.013.8Szpak, P. Fish bone chemistry and ultrastructure: implications for taphonomy and stable isotope analysis. J. Archaeol. Sci. 38, 3358–3372 (2011).Article 

    Google Scholar 
    Murray, D. C. et al. Scrapheap challenge: a novel bulk-bone metabarcoding method to investigate ancient DNA in faunal assemblages. Sci. Rep. 3, 3371 (2013).Article 

    Google Scholar 
    Møhl, J. in From Middle Ages to Colonial Times (ed. Gulløv, H. C.) 495–501 (Kommissionen for videnskabelige undersøgelser i Grønland, 1980).Møhl, U. Animal Bones from Itivnera, West Greenland: A Reindeer Hunting Site of the Sarqaq Culture (C. A. Reitzels Forlag, 1972).Stat, M. et al. Ecosystem biomonitoring with eDNA: metabarcoding across the tree of life in a tropical marine environment. Sci. Rep. 7, 12240 (2017).Article 

    Google Scholar 
    Arneborg, J. et al. Norse Greenland Dietary Economy ca. AD 980–ca. AD 1450: introduction. J. North Atl. S3, 1–39 (2012).
    Google Scholar 
    Whitridge, P. Zen fish: a consideration of the discordance between artifactual and zooarchaeological indicators of Thule Inuit fish use. J. Anthropol. Archaeol. 20, 3–72 (2001).Article 

    Google Scholar 
    Seersholm, F. V. et al. Rapid range shifts and megafaunal extinctions associated with late Pleistocene climate change. Nat. Commun. 11, 2770 (2020).Seersholm, F. V. et al. Ancient DNA preserved in small bone fragments from the P.W. Lund collection. Ecol. Evol. 11, 2064–2071 (2021).Article 

    Google Scholar 
    Wheeler, A. & Jones, A. K. J. Fishes (Cambridge Manuals in Archaeology) (Cambridge Univ. Press, 1989).Gotfredsen, A. B. Former occurrences of geese (Genera Anser and Branta) in ancient West Greenland: morphological and biometric approaches. Acta Zool. 45, 179–204 (2002).
    Google Scholar 
    Gotfredsen, A. B. & Møbjerg, T. Nipisat—A Saqqaq Culture Site in Sissimut, Central West Greenland (Museum Tusculanum Press, 2004).Bockstoce, J. R. On the development of whaling in the western Thule culture. Folk 18, 41–45 (1976).
    Google Scholar 
    Ferguson, S. H., Higdon, J. W., Hall, P. A., Hansen, R. G. & Doniol-Valcroze, T. Developing a precautionary management approach for the eastern Canada–west Greenland population of bowhead whales (Balaena mysticetus). Front. Mar. Sci. 8, 709989 (2021).Eschricht, D. F. Undersögelser over Hvaldyrene (Bianco Lunos Bogtrykkeri, 1846).Mikkelsen, N. et al. European trading, whaling and climate history of west Greenland documented by historical records, drones and marine sediments. Geol. Surv. Den. Greenl. Bull. 41, 67–70 (2018).
    Google Scholar 
    Borge, T., Bachmann, L., Bjørnstad, G. & Wiig, Ø. Genetic variation in Holocene bowhead whales from Svalbard. Mol. Ecol. 16, 2223–2235 (2007).CAS 
    Article 

    Google Scholar 
    LeDuc, R. G. Mitochondrial genetic variation in bowhead whales in the western Arctic. J. Cetacean Res. Manag. 10, 93–97 (2008).
    Google Scholar 
    McLeod, B. A. Examination of ten thousand years of mitochondrial DNA diversity and population demographics in bowhead whales (Balaena mysticetus) of the Central Canadian Arctic. Mar. Mammal. Sci. 28, 426–443 (2012).Article 

    Google Scholar 
    Foote, A. D. et al. Ancient DNA reveals that bowhead whale lineages survived Late Pleistocene climate change and habitat shifts. Nat. Commun. 4, 1677 (2013).Article 

    Google Scholar 
    Meldgaard, M. The Greenland Caribou—Zoogeography, Taxonomy, and Population Dynamics (Museum Tusculanum Press, 1986).Meldgaard, M. New perspectives on the zoogeography of the Greenlandic caribou (Rangifer tarandus). In Proc. 4th North American Caribou Workshop (eds Butler, C. & Mahoney, S. P.) 37–63 (Newfoundland and Labrador Wildlife Division, 1991).Solazzo, C., Fitzhugh, W., Kaplan, S., Potter, C. & Dyer, J. M. Molecular markers in keratins from Mysticeti whales for species identification of baleen in museum and archaeological collections. PLoS ONE 12, e0183053 (2017).Article 

    Google Scholar 
    Nowacek, D. P. et al. Buoyant balaenids: the ups and downs of buoyancy in right whales. Proc. R. Soc. B 268, 1811–1816 (2001).CAS 
    Article 

    Google Scholar 
    Hollesen, J. et al. Climate change and the deteriorating archaeological and environmental archives of the Arctic. Antiquity 92, 573–586 (2018).Article 

    Google Scholar 
    Hollesen, J. et al. Predicting the loss of organic archaeological deposits at a regional scale in Greenland. Sci. Rep. 9, 9097 (2019).Matthiesen, H., Høier Eriksen, A. M., Hollesen, J. & Collins, M. Bone degradation at five Arctic archaeological sites: quantifying the importance of burial environment and bone characteristics. J. Archaeol. Sci. 125, 105296 (2021).Seersholm, F. V. et al. Subsistence practices, past biodiversity, and anthropogenic impacts revealed by New Zealand-wide ancient DNA survey. Proc. Natl Acad. Sci. USA https://doi.org/10.1073/pnas.1803573115 (2018).Dabney, J. et al. Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments. Proc. Natl Acad. Sci. USA 110, 15758–63 (2013).CAS 
    Article 

    Google Scholar 
    Boyer, F. et al. obitools: a unix-inspired software package for DNA metabarcoding. Mol. Ecol. Resour. 16, 176–182 (2016).CAS 
    Article 

    Google Scholar 
    Rognes, T., Flouri, T., Nichols, B., Quince, C. & Mahé, F. VSEARCH: a versatile open source tool for metagenomics. PeerJ 4, e2584 (2016).Article 

    Google Scholar 
    Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).CAS 
    Article 

    Google Scholar 
    Dyke, A., Moore, A. & Robertson, L. Deglaciation of North America (Geological Survey of Canada, 2003).Dyke, A. S. An outline of North American deglaciation with emphasis on central and northern Canada. Dev. Quat. Sci. 2, 373–424 (2004).
    Google Scholar 
    Gansauge, M. & Meyer, M. Single-stranded DNA library preparation for the sequencing of ancient or damaged DNA. Nat. Protoc. 8, 737–748 (2013).Grealy, A. et al. Eggshell palaeogenomics: palaeognath evolutionary history revealed through ancient nuclear and mitochondrial DNA from Madagascan elephant bird (Aepyornis sp.) eggshell. Mol. Phylogenet. Evol. 109, 151–163 (2017).CAS 
    Article 

    Google Scholar 
    Lindgreen, S. AdapterRemoval: easy cleaning of next generation sequencing reads. BMC Res. Notes 5, 337 (2012).Article 

    Google Scholar 
    Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).CAS 
    Article 

    Google Scholar  More

  • in

    Genetic and particle modelling approaches to assessing population connectivity in a deep sea lobster

    Farmery, A. K., Hendrie, G. A., O’Kane, G., McManus, A. & Green, B. S. Sociodemographic variation in consumption patterns of sustainable and nutritious seafood in Australia. Front. Nutr. 5, 118. https://doi.org/10.3389/fnut.2018.00118 (2018).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Guillen, J. et al. Global seafood consumption footprint. Ambio 48, 111–122. https://doi.org/10.1007/s13280-018-1060-9 (2019).Article 
    PubMed 

    Google Scholar 
    Norse, E. A. et al. Sustainability of deep-sea fisheries. Mar. Policy 36, 307–320. https://doi.org/10.1016/j.marpol.2011.06.008 (2012).Article 

    Google Scholar 
    Baco, A. R. et al. A synthesis of genetic connectivity in deep-sea fauna and implications for marine reserve design. Mol. Ecol. 25, 3276–3298. https://doi.org/10.1111/mec.13689 (2016).Article 
    PubMed 

    Google Scholar 
    Victorero, L., Watling, L., Deng Palomares, M. L. & Nouvian, C. Out of sight, but within reach: A global history of bottom-trawled deep-sea fisheries from > 400 m depth. Front. Mar. Sci. 5, 98. https://doi.org/10.3389/fmars.2018.00098 (2018).Article 

    Google Scholar 
    Cowen, R. K. & Sponaugle, S. Larval dispersal and marine population connectivity. Ann. Rev. Mar. Sci. 1, 443–466. https://doi.org/10.1146/annurev.marine.010908.163757 (2009).Article 
    PubMed 

    Google Scholar 
    Taylor, M. L. & Roterman, C. N. Invertebrate population genetics across Earth’s largest habitat: The deep-sea floor. Mol. Ecol. 26, 4872–4896. https://doi.org/10.1111/mec.14237 (2017).CAS 
    Article 
    PubMed 

    Google Scholar 
    Allendorf, F. W., England, P. R., Luikart, G., Ritchie, P. A. & Ryman, N. Genetic effects of harvest on wild animal populations. Trends Ecol. Evol. 23, 327–337. https://doi.org/10.1016/j.tree.2008.02.008 (2008).Article 
    PubMed 

    Google Scholar 
    Carreras, C. et al. Population genomics of an endemic Mediterranean fish: Differentiation by fine scale dispersal and adaptation. Sci. Rep. 7, 43417. https://doi.org/10.1038/srep43417 (2017).ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Coleman, F. C. & Williams, S. L. Overexploiting marine ecosystem engineers: Potential consequences for biodiversity. Trends Ecol. Evol. 17, 40–44. https://doi.org/10.1016/S0169-5347(01)02330-8 (2002).Article 

    Google Scholar 
    Neubauer, P., Jensen, O. P., Hutchings, J. A. & Baum, J. K. Resilience and recovery of overexploited marine populations. Science 340, 347–349. https://doi.org/10.1126/science.1230441 (2013).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Ovenden, J. R., Berry, O., Welch, D. J., Buckworth, R. C. & Dichmont, C. M. Ocean’s eleven: A critical evaluation of the role of population, evolutionary and molecular genetics in the management of wild fisheries. Fish Fish. 16, 125–159. https://doi.org/10.1111/faf.12052 (2015).Article 

    Google Scholar 
    Pinsky, M. L. & Palumbi, S. R. Meta-analysis reveals lower genetic diversity in overfished populations. Mol. Ecol. 23, 29–39. https://doi.org/10.1111/mec.12509 (2014).Article 
    PubMed 

    Google Scholar 
    Sundqvist, L., Keenan, K., Zackrisson, M., Prodöhl, P. & Kleinhans, D. Directional genetic differentiation and relative migration. Ecol. Evol. 6, 3461–3475. https://doi.org/10.1002/ece3.2096 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Waples, R. S. et al. Guidelines for genetic data analysis. J. Cetac. Res. Manag. 18, 33–80 (2018).ADS 

    Google Scholar 
    Hauser, L., Adcock, G. J., Smith, P. J., Bernal Ramírez, J. H. & Carvalho, G. R. Loss of microsatellite diversity and low effective population size in an overexploited population of New Zealand snapper (Pagrus auratus). Proc. Natl. Acad. Sci. 99, 11742–11747. https://doi.org/10.1073/pnas.172242899 (2002).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Laikre, L., Palm, S. & Ryman, N. Genetic population structure of fishes: Implications for coastal zone management. AMBIO A J. Hum. Environ. 34, 111–119. https://doi.org/10.1579/0044-7447-34.2.111 (2005).Article 

    Google Scholar 
    Gaggiotti, O. E. Population genetic models of source–sink metapopulations. Theor. Popul. Biol. 50, 178–208. https://doi.org/10.1006/tpbi.1996.0028 (1996).CAS 
    Article 
    PubMed 
    MATH 

    Google Scholar 
    Hughes, A. R., Inouye, B. D., Johnson, M. T. J., Underwood, N. & Vellend, M. Ecological consequences of genetic diversity. Ecol. Lett. 11, 609–623. https://doi.org/10.1111/j.1461-0248.2008.01179.x (2008).Article 
    PubMed 

    Google Scholar 
    Bracco, A., Liu, G., Galaska, M. P., Quattrini, A. M. & Herrera, S. Integrating physical circulation models and genetic approaches to investigate population connectivity in deep-sea corals. J. Mar. Syst. 198, 103189. https://doi.org/10.1016/j.jmarsys.2019.103189 (2019).Article 

    Google Scholar 
    Liu, S.-Y.V., Hsin, Y.-C. & Cheng, Y.-R. Using particle tracking and genetic approaches to infer population connectivity in the deep-sea scleractinian coral Deltocyathus magnificus in the South China sea. Deep Sea Res. Part I 161, 103297. https://doi.org/10.1016/j.dsr.2020.103297 (2020).Article 

    Google Scholar 
    Dambach, J., Raupach, M. J., Leese, F., Schwarzer, J. & Engler, J. O. Ocean currents determine functional connectivity in an Antarctic deep-sea shrimp. Mar. Ecol. 37, 1336–1344. https://doi.org/10.1111/maec.12343 (2016).ADS 
    CAS 
    Article 

    Google Scholar 
    Selkoe, K. A., Henzler, C. M. & Gaines, S. D. Seascape genetics and the spatial ecology of marine populations. Fish Fish. 9, 363–377. https://doi.org/10.1111/j.1467-2979.2008.00300.x (2008).Article 

    Google Scholar 
    Yan, R.-J., Schnabel, K. E., Rowden, A. A., Guo, X.-Z. & Gardner, J. P. A. Population structure and genetic connectivity of squat lobsters (Munida Leach, 1820) associated with vulnerable marine ecosystems in the southwest Pacific Ocean. Front. Mar. Sci. https://doi.org/10.3389/fmars.2019.00791 (2020).Article 

    Google Scholar 
    Breusing, C. et al. Biophysical and population genetic models predict the presence of “phantom” stepping stones connecting Mid-Atlantic Ridge vent ecosystems. Curr. Biol. 26, 2257–2267. https://doi.org/10.1016/j.cub.2016.06.062 (2016).CAS 
    Article 
    PubMed 

    Google Scholar 
    Fisheries New Zealand. Fisheries Assessment: Scampi (SCI). https://fs.fish.govt.nz/Page.aspx?pk=113&dk=24443 (2017).Botsford, L. W. et al. Connectivity, sustainability, and yield: Bridging the gap between conventional fisheries management and marine protected areas. Rev. Fish Biol. Fish. 19, 69–95. https://doi.org/10.1007/s11160-008-9092-z (2009).Article 

    Google Scholar 
    NIWA. Annual Distribution of Scampi. Ministry for Primary Industries, New Zealand. https://mpi.maps.arcgis.com/home/item.html?id=97da6c1a912b45a8855bf741211f5911 (2016).Heasman, K. G. & Jeffs, A. G. Fecundity and potential juvenile production for aquaculture of the New Zealand scampi, Metanephrops challengeri (Balss, 1914) (Decapoda: Nephropidae). Aquaculture 511, 634184. https://doi.org/10.1016/j.aquaculture.2019.05.069 (2019).Article 

    Google Scholar 
    Smith, P. J. Allozyme variation in scampi (Metanephrops challengeri) fisheries around New Zealand. NZ J. Mar. Freshw. Res. 33, 491–497. https://doi.org/10.1080/00288330.1999.9516894 (1999).Article 

    Google Scholar 
    Berry, P. The biology of Nephrops andamanicus Wood-Mason (Decapoda, Reptantia). Report No. 22, 1–55 (South African Association for Marine Biological Research, Oceanographic Research Institute, Durban, South Africa, 1969).Major, R. N. & Jeffs, A. G. Orientation and food search behaviour of a deep sea lobster in turbulent versus laminar odour plumes. Helgol. Mar. Res. 71, 9. https://doi.org/10.1186/s10152-017-0489-8 (2017).Article 

    Google Scholar 
    Tuck, I. D., Parsons, D. M., Hartill, B. W. & Chiswell, S. M. Scampi (Metanephrops challengeri) emergence patterns and catchability. ICES J. Mar. Sci. 72, i199–i210. https://doi.org/10.1093/icesjms/fsu244 (2015).Article 

    Google Scholar 
    Chiswell, S. M. & Booth, J. D. Sources and sinks of larval settlement in Jasus edwardsii around New Zealand: Where do larvae come from and where do they go?. Mar. Ecol. Prog. Ser. 354, 201–217. https://doi.org/10.3354/meps07217 (2008).ADS 
    Article 

    Google Scholar 
    Silva, C. N. S., Macdonald, H. S., Hadfield, M. G., Cryer, M. & Gardner, J. P. A. Ocean currents predict fine-scale genetic structure and source-sink dynamics in a marine invertebrate coastal fishery. ICES J. Mar. Sci. 76, 1007–1018. https://doi.org/10.1093/icesjms/fsy201 (2019).Article 

    Google Scholar 
    Singh, S. P., Groeneveld, J. C., Hart-Davis, M. G., Backeberg, B. C. & Willows-Munro, S. Seascape genetics of the spiny lobster Panulirus homarus in the Western Indian Ocean: Understanding how oceanographic features shape the genetic structure of species with high larval dispersal potential. Ecol. Evol. 8, 12221–12237. https://doi.org/10.1002/ece3.4684 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Singh, S. P., Groeneveld, J. C. & Willows-Munro, S. Between the current and the coast: Genetic connectivity in the spiny lobster Panulirus homarus rubellus, despite potential barriers to gene flow. Mar. Biol. 166, 36. https://doi.org/10.1007/s00227-019-3486-4 (2019).Article 

    Google Scholar 
    Thomas, L. & Bell, J. J. Testing the consistency of connectivity patterns for a widely dispersing marine species. Heredity 111, 345–354. https://doi.org/10.1038/hdy.2013.58 (2013).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Baeza, J. A., Holstein, D., Umaña-Castro, R. & Mejía-Ortíz, L. M. Population genetics and biophysical modeling inform metapopulation connectivity of the Caribbean king crab Maguimithrax spinosissimus. Mar. Ecol. Prog. Ser. 610, 83–97 (2019).ADS 
    CAS 
    Article 

    Google Scholar 
    Hedgecock, D., Barber, P. H. & Edmands, S. Genetic approaches to measuring connectivity. Oceanography 20, 70–79 (2007).Article 

    Google Scholar 
    Jahnke, M. & Jonsson, P. R. Biophysical models of dispersal contribute to seascape genetic analyses. Philos. Trans. R. Soc. B Biol. Sci. 377, 20210024. https://doi.org/10.1098/rstb.2021.0024 (2022).Article 

    Google Scholar 
    Sebastian, W. et al. Genomic investigations provide insights into the mechanisms of resilience to heterogeneous habitats of the Indian Ocean in a pelagic fish. Sci. Rep. 11, 20690. https://doi.org/10.1038/s41598-021-00129-5 (2021).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lal, M. M., Southgate, P. C., Jerry, D. R., Bosserelle, C. & Zenger, K. R. A parallel population genomic and hydrodynamic approach to fishery management of highly-dispersive marine invertebrates: The case of the Fijian black-lip pearl oyster Pinctada margaritifera. PLoS ONE 11, e0161390. https://doi.org/10.1371/journal.pone.0161390 (2016).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Xu, T. et al. Hidden historical habitat-linked population divergence and contemporary gene flow of a deep-sea patellogastropod limpet. Mol. Biol. Evol. 38, 5640–5654. https://doi.org/10.1093/molbev/msab278 (2021).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    de Souza, J. M. A. C. et al. Moana Ocean Hindcast—A 25+ years simulation for New Zealand Waters using the ROMS v3.9 model. EGUsphere https://doi.org/10.5194/egusphere-2022-41 (2022).Norrie, C., Dunphy, B., Roughan, M., Weppe, S. & Lundquist, C. Spill-over from aquaculture may provide a larval subsidy for the restoration of mussel reefs. Aquac. Environ. Interact. 12, 231–249 (2020).Article 

    Google Scholar 
    Larsson, J. et al. Regional genetic differentiation in the blue mussel from the Baltic Sea area. Estuar. Coast. Shelf Sci. 195, 98–109. https://doi.org/10.1016/j.ecss.2016.06.016 (2017).ADS 
    Article 

    Google Scholar 
    Nicolle, A. et al. Modelling larval dispersal of Pecten maximus in the English Channel: A tool for the spatial management of the stocks. ICES J. Mar. Sci. 74, 1812–1825. https://doi.org/10.1093/icesjms/fsw207 (2017).Article 

    Google Scholar 
    Hold, N. et al. Using biophysical modelling and population genetics for conservation and management of an exploited species, Pecten maximus L. Fish. Oceanogr. 30, 740–756. https://doi.org/10.1111/fog.12556 (2021).Article 

    Google Scholar 
    Truelove, N. K. et al. Biophysical connectivity explains population genetic structure in a highly dispersive marine species. Coral Reefs 36, 233–244. https://doi.org/10.1007/s00338-016-1516-y (2017).ADS 
    Article 

    Google Scholar 
    Busch, K. et al. Population connectivity of fan-shaped sponge holobionts in the deep Cantabrian Sea. Deep Sea Res. Part I 167, 103427. https://doi.org/10.1016/j.dsr.2020.103427 (2021).Article 

    Google Scholar 
    Ross, P. M., Hogg, I. D., Pilditch, C. A. & Lundquist, C. J. Phylogeography of New Zealand’s coastal benthos. NZ J. Mar. Freshw. Res. 43, 1009–1027. https://doi.org/10.1080/00288330.2009.9626525 (2009).Article 

    Google Scholar 
    Tuck, I. D. Characterisation and a length-based assessment model for scampi (Metanephrops challengeri) at the Auckland Islands (SCI 6A). Report No. 2015/21, 160 (Ministry for Primary Industries, Wellington, 2015).Verry, A. J. F., Walton, K., Tuck, I. D. & Ritchie, P. A. Genetic structure and recent population expansion in the commercially harvested deepsea decapod, Metanephrops challengeri (Crustacea: Decapoda). NZ J. Mar. Freshw. Res. 54, 251–270. https://doi.org/10.1080/00288330.2019.1707696 (2020).CAS 
    Article 

    Google Scholar 
    Selkoe, K. A. et al. A decade of seascape genetics: Contributions to basic and applied marine connectivity. Mar. Ecol. Prog. Ser. 554, 1–19. https://doi.org/10.3354/meps11792 (2016).ADS 
    Article 

    Google Scholar 
    Hare, M. P. et al. Understanding and estimating effective population size for practical application in marine species management. Conserv. Biol. 25, 438–449. https://doi.org/10.1111/j.1523-1739.2010.01637.x (2011).Article 
    PubMed 

    Google Scholar 
    Ashry, N. A. Plant biodiversity and biotechnology. In From Plant Genomics to Plant Biotechnology (eds Poltronieri, P. et al.) 205–222 (Woodhead Publishing, 2013).Chapter 

    Google Scholar 
    Sgrò, C. M., Lowe, A. J. & Hoffmann, A. A. Building evolutionary resilience for conserving biodiversity under climate change. Evol. Appl. 4, 326–337. https://doi.org/10.1111/j.1752-4571.2010.00157.x (2011).Article 
    PubMed 

    Google Scholar 
    Kerr, L. A., Cadrin, S. X. & Secor, D. H. Simulation modelling as a tool for examining the consequences of spatial structure and connectivity on local and regional population dynamics. ICES J. Mar. Sci. 67, 1631–1639. https://doi.org/10.1093/icesjms/fsq053 (2010).Article 

    Google Scholar 
    Carroll, E. L. et al. Perturbation drives changing metapopulation dynamics in a top marine predator. Proc. R. Soc. B Biol. Sci. 287, 20200318. https://doi.org/10.1098/rspb.2020.0318 (2020).Article 

    Google Scholar 
    Chiswell, S. M., Bostock, H. C., Sutton, P. J. H. & Williams, M. J. M. Physical oceanography of the deep seas around New Zealand: A review. NZ J. Mar. Freshw. Res. 49, 286–317. https://doi.org/10.1080/00288330.2014.992918 (2015).Article 

    Google Scholar 
    Chiswell, S. M. & Roemmich, D. The East Cape Current and two eddies: A mechanism for larval retention?. NZ J. Mar. Freshw. Res. 32, 385–397. https://doi.org/10.1080/00288330.1998.9516833 (1998).Article 

    Google Scholar 
    Condie, S. & Condie, R. Retention of plankton within ocean eddies. Glob. Ecol. Biogeogr. 25, 1264–1277. https://doi.org/10.1111/geb.12485 (2016).Article 

    Google Scholar 
    Lesser, J. H. R. Phyllosoma larvae of Jasus edwardsii (Hutton) (Crustacea: Decapoda: Palinuridae) and their distribution off the east coast of the North Island, New Zealand. NZ J. Mar. Freshw. Res. 12, 357–370. https://doi.org/10.1080/00288330.1978.9515763 (1978).Article 

    Google Scholar 
    Kawecki, T. J. Ecological and evolutionary consequences of source-sink population dynamics. In Ecology, Genetics and Evolution of Metapopulations (eds Hanski, I. & Gaggiotti, O. E.) 387–414 (Academic Press, 2004).Chapter 

    Google Scholar 
    Figueira, W. F. & Crowder, L. B. Defining patch contribution in source-sink metapopulations: the importance of including dispersal and its relevance to marine systems. Popul. Ecol. 48, 215–224. https://doi.org/10.1007/s10144-006-0265-0 (2006).Article 

    Google Scholar 
    Heinrichs, J. A. et al. Recent advances and current challenges in applying source-sink theory to species conservation. Curr. Landsc. Ecol. Rep. 4, 51–60. https://doi.org/10.1007/s40823-019-00039-3 (2019).Article 

    Google Scholar 
    Hastings, A. & Botsford, L. W. Persistence of spatial populations depends on returning home. Proc. Natl. Acad. Sci. 103, 6067–6072. https://doi.org/10.1073/pnas.0506651103 (2006).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Heinrichs, J. A., Lawler, J. J. & Schumaker, N. H. Intrinsic and extrinsic drivers of source-sink dynamics. Ecol. Evol. 6, 892–904. https://doi.org/10.1002/ece3.2029 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gilroy, J. J. & Edwards, D. P. Source-sink dynamics: A neglected problem for landscape-scale biodiversity conservation in the Tropics. Curr. Landsc. Ecol. Rep. 2, 51–60. https://doi.org/10.1007/s40823-017-0023-3 (2017).Article 

    Google Scholar 
    Lal, M. M., Bosserelle, C., Kishore, P. & Southgate, P. C. Understanding marine larval dispersal in a broadcast-spawning invertebrate: A dispersal modelling approach for optimising spat collection of the Fijian black-lip pearl oyster Pinctada margaritifera. PLoS ONE 15, e0234605. https://doi.org/10.1371/journal.pone.0234605 (2020).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Chassé, J. & Miller, R. J. Lobster larval transport in the southern Gulf of St. Lawrence. Fish. Oceanogr. 19, 319–338. https://doi.org/10.1111/j.1365-2419.2010.00548.x (2010).Article 

    Google Scholar 
    Lindegren, M., Andersen, K. H., Casini, M. & Neuenfeldt, S. A metacommunity perspective on source–sink dynamics and management: the Baltic Sea as a case study. Ecol. Appl. 24, 1820–1832. https://doi.org/10.1890/13-0566.1 (2014).Article 
    PubMed 

    Google Scholar 
    Tuck, I. D. et al. Estimating the abundance of scampi in SCI 6A (Auckland Islands) in 2013. Report No. 2015/10, 48 (Ministry for Primary Industries, 2015).Brierley, A. S. & Kingsford, M. J. Impacts of climate change on marine organisms and ecosystems. Curr. Biol. 19, R602–R614. https://doi.org/10.1016/j.cub.2009.05.046 (2009).CAS 
    Article 
    PubMed 

    Google Scholar 
    Caesar, L., Rahmstorf, S., Robinson, A., Feulner, G. & Saba, V. Observed fingerprint of a weakening Atlantic Ocean overturning circulation. Nature 556, 191–196. https://doi.org/10.1038/s41586-018-0006-5 (2018).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Thornalley, D. J. R. et al. Anomalously weak Labrador Sea convection and Atlantic overturning during the past 150 years. Nature 556, 227–230. https://doi.org/10.1038/s41586-018-0007-4 (2018).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    van Gennip, S. J. et al. Going with the flow: The role of ocean circulation in global marine ecosystems under a changing climate. Glob. Change Biol. 23, 2602–2617. https://doi.org/10.1111/gcb.13586 (2017).ADS 
    Article 

    Google Scholar 
    Bashevkin, S. M. et al. Larval dispersal in a changing ocean with an emphasis on upwelling regions. Ecosphere 11, e03015. https://doi.org/10.1002/ecs2.3015 (2020).Article 

    Google Scholar 
    Gerber, L. R., Mancha-Cisneros, M. D. M., O’Connor, M. I. & Selig, E. R. Climate change impacts on connectivity in the ocean: Implications for conservation. Ecosphere 5, 1–18. https://doi.org/10.1890/es13-00336.1 (2014).Article 

    Google Scholar 
    Hoegh-Gulderg, O. & Pearse, J. Temperature, food availability, and the development of marine invertebrate larvae. Am. Zool. 35, 415–425. https://doi.org/10.1093/icb/35.4.415 (1995).Article 

    Google Scholar 
    O’Connor, M. I. et al. Temperature control of larval dispersal and the implications for marine ecology, evolution, and conservation. Proc. Natl. Acad. Sci. USA 104, 1266–1271. https://doi.org/10.1073/pnas.0603422104 (2007).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Cetina-Heredia, P., Roughan, M., van Sebille, E., Feng, M. & Coleman, M. A. Strengthened currents override the effect of warming on lobster larval dispersal and survival. Glob. Change Biol. 21, 4377–4386. https://doi.org/10.1111/gcb.13063 (2015).ADS 
    Article 

    Google Scholar 
    Borja, A. et al. Past and future grand challenges in marine ecosystem ecology. Front. Mar. Sci. https://doi.org/10.3389/fmars.2020.00362 (2020).Article 

    Google Scholar 
    Ogilvie, S. et al. Mātauranga Māori driving innovation in the New Zealand scampi fishery. NZ J. Mar. Freshw. Res. 52, 590–602. https://doi.org/10.1080/00288330.2018.1532441 (2018).Article 

    Google Scholar 
    Andrews, S. FastQC: A quality control tool for high throughput sequence data v. 0.11.7 (Babraham Bioinformatics, 2010). http://www.bioinformatics.babraham.ac.uk/projects/fastqc.Rochette, N. C., Rivera-Colón, A. G. & Catchen, J. M. Stacks 2: Analytical methods for paired-end sequencing improve RADseq-based population genomics. Mol. Ecol. 28, 4737–4754. https://doi.org/10.1111/mec.15253 (2019).CAS 
    Article 
    PubMed 

    Google Scholar 
    Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158. https://doi.org/10.1093/bioinformatics/btr330 (2011).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    R Core Team. R: A Language and Environment for Statistical Computing v. 4.1.0 (R Studio v1.4.1106) (R Foundation for Statistical Computing, Vienna, Austria, 2021). https://www.R-project.org/.Díaz-Arce, N. & Rodríguez-Ezpeleta, N. Selecting RAD-seq data analysis parameters for population genetics: The more the better?. Front. Genet. 10, 533. https://doi.org/10.3389/fgene.2019.00533 (2019).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Potapov, V. & Ong, J. L. Examining sources of error in PCR by single-molecule sequencing. PLoS ONE 12, e0169774. https://doi.org/10.1371/journal.pone.0169774 (2017).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Goudet, J. & Jombart, T. hierfstat: Estimation and Tests of Hierarchical F-Statistics v. 0.04-22 (Comprehensive R Archive Network (CRAN), 2015). https://CRAN.R-project.org/package=hierfstat.Nei, M. Molecular Evolutionary Genetics (Columbia University Press, 1987).Book 

    Google Scholar 
    Nei, M. & Chesser, R. K. Estimation of fixation indices and gene diversities. Ann. Hum. Genet. 47, 253–259. https://doi.org/10.1111/j.1469-1809.1983.tb00993.x (1983).CAS 
    Article 
    PubMed 
    MATH 

    Google Scholar 
    Archer, F. I., Adams, P. E. & Schneiders, B. B. stratag: An R package for manipulating, summarizing and analysing population genetic data. Mol. Ecol. Resour. 17, 5–11. https://doi.org/10.1111/1755-0998.12559 (2017).CAS 
    Article 
    PubMed 

    Google Scholar 
    Kamvar, Z. N., Tabima, J. F. & Grünwald, N. J. Poppr: An R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2, e281. https://doi.org/10.7717/peerj.281 (2014).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kamvar, Z. N., Brooks, J. C. & Grünwald, N. J. Novel R tools for analysis of genome-wide population genetic data with emphasis on clonality. Front. Genet. 6, 208. https://doi.org/10.3389/fgene.2015.00208 (2015).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Jombart, T. adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405. https://doi.org/10.1093/bioinformatics/btn129 (2008).CAS 
    Article 
    PubMed 

    Google Scholar 
    Jombart, T. & Ahmed, I. adegenet 1.3–1: New tools for the analysis of genome-wide SNP data. Bioinformatics 27, 3070–3071. https://doi.org/10.1093/bioinformatics/btr521 (2011).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Miller, J. M., Cullingham, C. I. & Peery, R. M. The influence of a priori grouping on inference of genetic clusters: Simulation study and literature review of the DAPC method. Heredity 125, 269–280. https://doi.org/10.1038/s41437-020-0348-2 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Keenan, K., McGinnity, P., Cross, T. F., Crozier, W. W. & Prodöhl, P. A. diveRsity: An R package for the estimation and exploration of population genetics parameters and their associated errors. Methods Ecol. Evol. 4, 782–788. https://doi.org/10.1111/2041-210x.12067 (2013).Article 

    Google Scholar 
    Nei, M. Analysis of gene diversity in subdivided populations. Proc. Natl. Acad. Sci. 70, 3321–3323. https://doi.org/10.1073/pnas.70.12.3321 (1973).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar 
    Dagestad, K. F., Röhrs, J., Breivik, Ø. & Ådlandsvik, B. OpenDrift v1.0: A generic framework for trajectory modelling. Geosci. Model Dev. 11, 1405–1420. https://doi.org/10.5194/gmd-11-1405-2018 (2018).ADS 
    Article 

    Google Scholar 
    Jeffs, A., Daniels, C. & Heasman, K. In Fisheries and Aquaculture: Natural History of Crustacea, Vol. 9 (eds Lovrich, G. & Thiel, M.) 285–311 (Oxford University Press, 2020).Lundquist, C. J., Oldman, J. W. & Lewis, M. J. Predicting suitability of cockle Austrovenus stutchburyi restoration sites using hydrodynamic models of larval dispersal. NZ J. Mar. Freshw. Res. 43, 735–748. https://doi.org/10.1080/00288330909510038 (2009).Article 

    Google Scholar 
    Lundquist, C. J., Thrush, S. F., Oldman, J. W. & Senior, A. K. Limited transport and recolonization potential in shallow tidal estuaries. Limnol. Oceanogr. 49, 386–395. https://doi.org/10.4319/lo.2004.49.2.0386 (2004).ADS 
    Article 

    Google Scholar 
    Okubo, A. & Ebbesmeyer, C. C. Determination of vorticity, divergence, and deformation rates from analysis of drogue observations. Deep-Sea Res. Oceanogr. Abstr. 23, 349–352. https://doi.org/10.1016/0011-7471(76)90875-5 (1976).ADS 
    Article 

    Google Scholar 
    Pierce, D. ncdf4: Interface to Unidata netCDF (Version 4 or Earlier) Format Data Files v. 1.17 (Comprehensive R Archive Network (CRAN), 2019). https://CRAN.R-project.org/package=ncdf4.Coelho, S. C. C., Gherardi, D. F. M., Gouveia, M. B. & Kitahara, M. V. Western boundary currents drive sun-coral (Tubastraea spp.) coastal invasion from oil platforms. Sci. Rep. 12, 5286. https://doi.org/10.1038/s41598-022-09269-8 (2022).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Demmer, J. et al. The role of wind in controlling the connectivity of blue mussels (Mytilus edulis L.) populations. Mov. Ecol. 10, 3. https://doi.org/10.1186/s40462-022-00301-0 (2022).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Atalah, J., South, P. M., Briscoe, D. K. & Vennell, R. Inferring parental areas of juvenile mussels using hydrodynamic modelling. Aquaculture 555, 738227. https://doi.org/10.1016/j.aquaculture.2022.738227 (2022).Article 

    Google Scholar 
    McGeady, R., Lordan, C. & Power, A. M. Long-term interannual variability in larval dispersal and connectivity of the Norway lobster (Nephrops norvegicus) around Ireland: When supply-side matters. Fish. Oceanogr. 31, 255–270. https://doi.org/10.1111/fog.12576 (2022).Article 

    Google Scholar 
    Pante, E. & Simon-Bouhet, B. marmap: A package for importing, plotting and analyzing bathymetric and topographic data in R. PLoS ONE 8, e73051. https://doi.org/10.1371/journal.pone.0073051 (2013).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2016).MATH 

    Google Scholar 
    Becker, R. A., Wilks, A. R. & Brownrigg, R. mapdata: Extra Map Databases v. 2.3.0 (Comprehensive R Archive Network (CRAN), 2018). https://CRAN.R-project.org/package=mapdata.McIlroy, D., Brownrigg, R., Minka, T. P. & Bivan, R. mapproj: Map Projections v. 1.2.7 (Comprehensive R Archive Network (CRAN), 2020). https://CRAN.R-project.org/package=mapproj.South, A. rnaturalearth: World Map Data from Natural Earth v. 0.1.0 (Comprehensive R Archive Network (CRAN), 2017). https://CRAN.R-project.org/package=rnaturalearth. More

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    A pachyderm perfume: odour encodes identity and group membership in African elephants

    Wyatt, T. Pheromones and Animal Behavior: Communication by Smell and Taste (Cambridge University Press, 2003).Book 

    Google Scholar 
    Wyatt, T. D. Fifty years of pheromones. Nature 457, 262–263 (2009).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Burgener, N., Dehnhard, M., Hofer, H. & East, M. Does anal gland scent signal identity in the spotted hyena?. Anim. Behav. 77, 707–715 (2009).Article 

    Google Scholar 
    Kent, L. & Tang-Martínez, Z. Evidence of individual odors and individual discrimination in the raccoon, Procyon lotor. J. Mamm. 95, 1254–1262 (2014).Article 

    Google Scholar 
    Klücklich, M., Weiß, B. M., Birkemere, C., Einspanier, A. & Widdig, A. Chemical cues of female fertility states in a non-human primate. Sci. Rep. 9, 9–12 (2019).
    Google Scholar 
    Setchell, J. M. et al. Chemical composition of scent-gland secretions in an Old World monkey (Mandrillus sphinx): Influence of sex, male status, and individual identity. Chem. Sens. 35, 205–220 (2010).CAS 
    Article 

    Google Scholar 
    Marneweck, C., Jurgens, A. & Shrader, A. M. Dung odours signal sex, age, territorial and oestrous state in white rhinos. Proc. R. Soc. B 284, 20162376 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Heth, G., Todrank, J., Busquet, N. & Baudoin, C. Genetic relatedness assessment through individual odour similarities (G-ratios) in mice. Biol. J. Lin. Soc. 78, 595–603 (2003).Article 

    Google Scholar 
    Heth, G., Todrank, J., Begall, S., Wegner, R. & Burda, H. Genetic relatedness discrimination in eusocial Cryptomys anselli mole-rats, Bathyergidae, Rodentia. Folia Zool. 53, 269–278 (2004).
    Google Scholar 
    Busquet, N. & Baudoin, C. Odour similarities as a basis for discriminating degrees of kinship in rodents: Evidence from Mus spicilegus. Anim. Behav. 70, 997–1002 (2005).Article 

    Google Scholar 
    Stoffel, M. A. et al. Chemical fingerprints encode mother–offspring similarity, colony membership, relatedness, and genetic quality in fur seals. PNAS 112(36), E5005–E5012 (2015).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Charpentier, M., Boulet, M. & Drea, C. Smelling right: The scent of male lemurs advertises genetic quality and relatedness. Mol. Ecol. 17, 3225–3233 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    Boulet, M., Charpentier, M. J. E. & Drea, C. M. Decoding an olfactory mechanism of kin recognition and inbreeding avoidance in primates. BMC Evol. Biol. 9, 281 (2009).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kean, E. F., Bruford, M., Russo, I. R., Müller, C. & Chadwick, E. Odour dialects among wild mammals. Sci. Rep. 7, 13593 (2017).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Wedekind, C., Seebeck, T., Bettens, F. & Paepke, A. J. MHC-dependent mate preferences in humans. Proc. Biol. Sci. 260, 245–249 (1995).CAS 
    PubMed 
    Article 

    Google Scholar 
    Penn, D. & Potts, W. K. Untrained mice discriminate MHC-determined odors. Phys. Behav. 64(3), 235–243 (1998).CAS 
    Article 

    Google Scholar 
    Sun, L. & Müller-Schwarze, D. Anal gland secretion codes for family membership in beaver. Behav. Ecol. Sociobiol. 44(3), 199–208 (1998).Article 

    Google Scholar 
    Bloss, J., Acree, T. E., Bloss, J. M., Hood, W. R. & Kunz, T. H. Potential use of chemical cues for colony-mate recognition in the big brown bat, Eptesicus fuscus. J. Chem. Ecol. 28(4), 819–834 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    Weiß, B. M. et al. A non-invasive method for sampling the body odour of mammals. Methods Ecol. Evol. 9, 420–429 (2018).Article 

    Google Scholar 
    O’Riain, M. J. & Jarvis, J. U. M. Colony member recognition and xenophobia in the naked mole-rat. Anim. Behav. 53, 487–498 (1997).Article 

    Google Scholar 
    Henkel, S. & Setchell, J. Group and kin recognition via olfactory cues in chimpanzees (Pan troglodytes). Proc. R. Soc. B. 285, 20181527 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Henkel, S., Lambides, A. R., Berger, A., Thomsen, R. & Widdig, A. Rhesus macaques (Macaca mulatta) recognize group membership via olfactory cues alone. Behav. Ecol. Sociobiol. 69, 2019–2034 (2015).Article 

    Google Scholar 
    Tzur, S., Todrank, J., Jürgens, A., Nevo, E. & Heth, G. Odour–genes covariance within a natural population of subterranean Spalax galili blind mole rats. Biol. J. Lin. Soc. 96, 483–490 (2009).Article 

    Google Scholar 
    Leclaire, S., Jacob, S., Greene, L. K., Dubay, G. R. & Drea, C. M. Social odours covary with bacterial community in the anal secretions of wild meerkats. Sci. Rep. 7, 1–13 (2017).CAS 
    Article 

    Google Scholar 
    Archie, E. & Theis, K. Animal behavior meets microbial ecology. Anim. Behav. 82, 425–436 (2011).Article 

    Google Scholar 
    Sukumar, R. The Living Elephants: Evolutionary Ecology, Behavior and Conservation (Oxford University Press, 2003).
    Google Scholar 
    Jachowski, D. The Amboseli Elephants: A long-term perspective on a long-lived mammal by C. J. Moss; H. Croze; P. C. Lee. J. Mammal. 93, 294–295 (2012).Article 

    Google Scholar 
    Slotow, R., van Dyk, G., Poole, J., Page, B. & Klocke, A. Older bull elephants control young males. Nature 408, 425–426 (2000).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Niimura, Y., Matsui, A. & Touhara, K. Extreme expansion of the olfactory receptor gene repertoire in African elephants and evolutionary dynamics of orthologous gene groups in 13 placental mammals. Genome Res. 24, 1485–1496 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Goodwin, T. E., Broederdorf, L. J. & Burkert, B. A. Chemical signals of elephant musth: Temporal aspects of microbially-mediated modifications. J. Chem. Ecol. 38, 81–87 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Schulte, B. A. & Rasmussen, L. E. L. Musth, sexual selection, testosterone and metabolites. In Advances in Chemical Communication in Vertebrates (eds Johnston, R. E. et al.) 383–397 (Plenum Press, New York, 1999).
    Google Scholar 
    Rasmussen, L. E. L. Chemical communication: An integral part of functional Asian elephant (Elephas maximus) society. Ecoscience 5, 410–426 (1998).Article 

    Google Scholar 
    Rasmussen, L. E. L. & Krishnamurthy, V. How chemical signals integrate Asian elephant society: The known and the unknown. Zool. Biol. 19, 405–423 (2000).CAS 
    Article 

    Google Scholar 
    Greenwood, D. R., Comesky, D., Hunt, M. B. & Rasmussen, L. E. L. Chirality in elephant pheromones. Nature 438, 1097–1098 (2005).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Clutton-Brock, T. H. & Huchard, E. Social competition and selection in males and females. Phil. Trans. R. Soc. 368, 20130074 (2013).CAS 
    Article 

    Google Scholar 
    Wittemyer, G. & Getz, W. M. Hierarchical dominance structure and social organization in African elephants Loxodonta africana. Anim. Behav. 73, 671–681 (2007).Article 

    Google Scholar 
    Moss, C. Elephant memories (William Morrow, 1988).
    Google Scholar 
    Buss, I. O., Rasmussen, L. E. L. & Smuts, G. L. Role of stress and individual recognition in the function of the African elephants’ temporal gland. Mammalia 40(3), 437–451 (1976).Article 

    Google Scholar 
    Wittemyer, G., Douglas-Hamilton, I. & Getz, W. M. The socioecology of elephants: Analysis of the processes creating multi-tiered social structures. Anim. Behav. 69(6), 1357–1371 (2005).Article 

    Google Scholar 
    Bates, L. A. et al. African elephants have expectations about the locations of out-of-sight family members. Biol. Lett. 4(1), 34–36 (2008).PubMed 
    Article 

    Google Scholar 
    Bates, L. A. et al. Elephants classify human ethnic groups by odor and garment color. Curr. Biol 17(22), 1938–1942 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Plotnik, J. M. et al. Elephants have a nose for quantity. PNAS 116(25), 12566–12571 (2019).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    de Silva, S., Schmid, V. & Wittemyer, G. Fission–fusion processes weaken dominance networks of female Asian elephants in a productive habitat. Behav. Ecol. https://doi.org/10.1093/beheco/arw153 (2016).Article 

    Google Scholar 
    Archie, E. A., Moss, C. J. & Alberts, S. C. The ties that bind: Genetic relatedness predicts the fission and fusion of social groups in wild African elephants. Proc. R. Soc. Lond. 273, 513–522 (2006).CAS 

    Google Scholar 
    Allen, C. R. B., Brent, L. J. N., Motsentwa, T., Weiss, M. N. & Croft, D. P. Importance of old bulls: Leaders and followers in collective movements of all-male groups in African savannah elephants (Loxodonta africana). Sci. Rep. https://doi.org/10.1038/s41598-020-70682-y (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Goodwin, T. et al. The Role of Bacteria in Chemical Signals of Elephant Musth. In Chemical Signals in Vertebrates Vol. 13 (eds Schulte, B. et al.) (Springer, 2016).
    Google Scholar 
    Wittemyer, G. et al. Where sociality and relatedness diverge: The genetic basis for hierarchical social organization in African elephants. Proc. Biol. Sci. 7(276), 3513–3521 (2009).
    Google Scholar 
    Stoeger, A. & Baotic, A. Information content and acoustic structure of male African elephant social rumbles. Sci. Rep. 6, 27585 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    McComb, K., Reby, D., Baker, L., Moss, C. & Sayialel, S. Long-distance communication of social identity in African elephants. Anim. Behav. 65, 317–329 (2003).Article 

    Google Scholar 
    Archie, E. A. et al. Behavioural inbreeding avoidance in wild African elephants. Molec. Ecol 16, 4138–4148 (2007).CAS 
    Article 

    Google Scholar 
    von Dürckheim, K. Olfaction and scent discrimination in African elephants. PhD thesis, Stellenbosch University, South Africa (2021).Goodwin, T. E. et al. African elephant sesquiterpenes. II. Identification and synthesis of new derivatives of 2,3-dihydrofarnesol. J. Nat. Prod. 65, 1319–1322 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    Goodwin, T. E. et al. Chemical analysis of African elephant urine: A search for putative pheromones. In Chemical Signals in Vertebrates 10 (eds Mason, R. T. et al.) 128–139 (Springer Press, 2005).Chapter 

    Google Scholar 
    Goodwin, T. E. et al. Insect pheromones and precursors in female African elephant urine. J. Chem. Ecol. 32, 1849–1853 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    Burger, B. V. Mammalian semiochemicals. In The chemistry of Pheromones and Other Semiochemicals II. Topics in Current Chemistry Vol. 240 (ed. Schulz, S.) 231–278 (Springer, 2005).
    Google Scholar 
    Charpentier, M. J. E., Barthes, N., Proffit, M., Bessière, J. M. & Grison, C. Critical thinking in the chemical ecology of mammalian communication: Roadmap for future studies. Funct. Ecol. 26, 769–774 (2012).Article 

    Google Scholar 
    Apps, P., Weldon, P. & Kramer, M. Chemical signals in terrestrial vertebrates: Search for design features. Nat. Prod. Rep. 32, 1131–1153 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Burgener, N., East, M., Hofer, H. & Dehnhard, M. Do spotted hyena scent marks code for clan membership? In Chemical Signals in Vertebrates XI (eds Hurst, J. L. et al.) 169–178 (Springer, 2008).Chapter 

    Google Scholar 
    Lukas, D. & Clutton-Brock, T. Social complexity and kinship in animal societies. Ecol. Lett. 21, 1129–1134. https://doi.org/10.1111/ele.13079 (2018).Article 
    PubMed 

    Google Scholar 
    Meyer, J. M., Goodwin, T. E. & Schulte, B. A. Intrasexual chemical communication and social responses of captive female African elephants, Loxodonta africana. Anim. Behav. 76, 163–174 (2008).Article 

    Google Scholar 
    Soltis, J., Leong, K. & Savage, A. African elephant vocal communication II: Rumble variation reflects the individual identity and emotional state of callers. Anim. Behav. 70(3), 589–599 (2005).Article 

    Google Scholar 
    Scordato, E. S. & Drea, C. M. Scents and sensibility: Information content of olfactory signals in the ringtailed lemur, Lemur catta. Anim. Behav. 73, 301–314 (2007).Article 

    Google Scholar 
    Palagi, E. & Dapporto, L. Beyond odor discrimination: Demonstrating individual recognition by scent in Lemur catta. Chem. Sens. 31, 437–443 (2006).Article 

    Google Scholar 
    Johnston, R. E., Derzie, A., Chiang, G., Jernigan, P. & Lee, H. C. Individual scent signatures in golden hamsters: Evidence for specialization of function. Anim. Behav. 45, 1061–1070 (1993).Article 

    Google Scholar 
    Coffin, H., Watters, J. & Mateo, J. Odor-based recognition of familiar and related conspecifics: A first test conducted on captive Humboldt Penguins (Spheniscus humboldti). PLoS ONE 6, e25002 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Leclaire, S. et al. An individual and a sex odor signature in kittiwakes? Study of the semiochemical composition of preen secretion and preen down feathers. Naturwissenschaften 98, 615–624 (2011).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    von Dürckheim, K. et al. African elephants (Loxodonta africana) display remarkable olfactory acuity in human scent matching to sample performance. Appl. Anim. Behav. 200, 123–129 (2018).Article 

    Google Scholar 
    Bates, L. A., Poole, J. H. & Byrne, R. W. Elephant cognition. Curr. Biol. 18, 544–546. https://doi.org/10.1016/j.cub.2008.04.019 (2008).CAS 
    Article 

    Google Scholar 
    Kean, E., Müller, C. & Chadwick, E. Otter scent signals age, sex, and reproductive status. Chem. Sens. 36, 555–564 (2011).CAS 
    Article 

    Google Scholar 
    Kioko, J., Taylor, K., Milne, H. J., Hayes, K. Z. & Kiffner, C. Temporal gland secretion in African elephants (Loxodonta africana). Mamm. Biol. 82, 34–44 (2017).Article 

    Google Scholar 
    Macdonald, E., Fernandez-Duque, E., Sian, E. & Hagey, L. Sex, age, and family differences in the chemical composition of owl monkey (Aotus nancymaae) subcaudal scent secretions. Am. J. Primatol. 70, 12–18 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    Zhang, J. et al. Potential chemosignals in the anogenital gland secretion of giant pandas, Ailuropoda melanoleuca, associated with sex and individual identity. J. Chem. Ecol. 34, 398–407 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    Theis, K. R. et al. Symbiotic bacteria appear to mediate hyena social odors. Proc. Natl. Acad. Sci. 110(49), 19832–19837 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Merritt, G. C., Goodrich, B. S., Hesterman, E. R. & Myktowycz, R. Microflora and volatile fatty acids present in the inguinal pouches of the wild rabbit, Oryctolagus cuniculus in Australia. J. Chem. Ecol. 8, 217–1225 (1982).Article 

    Google Scholar 
    Müller-Schwarze, D. & Heckman, S. The social role of scent in beaver (Castor canadensis). J. Chem. Ecol. 6, 81–95 (1980).Article 

    Google Scholar 
    Albone, E. S., Eglinton, G., Walker, J. M. & Ware, G. C. Anal sac secretion of red fox (Vulpes vulpes), its chemistry and microbiology: Comparison with anal sac secretion of lion (Panthera leo). Life Sci. 14, 387–400 (1974).CAS 
    PubMed 
    Article 

    Google Scholar 
    Gorman, M. L. A mechanism for individual recognition by odour in Herpestes auropunctatus (Carnivora: Viverridae). Anim. Behav. 24, 141–145 (1976).Article 

    Google Scholar 
    Theis, K. R., Schmidt, M. S. & Holekamp, K. E. Evidence for a bacterial mechanism for group-specific social odors among hyenas. Sci. Rep. 2, 615 (2012).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Theis, K. R., Heckla, A. L., Verge, J. R. & Holekamp, K. E. The ontogeny of pasting behavior in free-living spotted hyenas, Crocuta crocuta. In Chemical Signals in Vertebrates Vol. 11 (eds Hurst, J. L. et al.) 179–188 (Springer, 2008).
    Google Scholar 
    Chiyo, P. I. et al. The influence of social structure, habitat, and host traits on the transmission of Escherichia coli in wild elephants. PLoS ONE 9(4), e93408 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Archie, E. A., Moss, C. J. & Alberts, S. C. Characterization of tetranucleotide microsatellite loci in the African Savannah elephant (Loxodonta africana africana). Mol. Ecol. Notes. 3, 244–246 (2003).CAS 
    Article 

    Google Scholar 
    Comstock, K. E., Wasser, S. K. & Ostrander, E. A. Polymorphic microsatellite DNA loci identified in the African elephant (Loxodonta africana). Mol. Ecol. 9, 1004–1006 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    Eggert, L. S., Eggert, J. A. & Woodruff, D. S. Estimating population sizes for elusive animals: The forest elephants of Kakum National Park, Ghana. Mol. Ecol. 12, 1389–1402 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    Toonen, R. J. & Hughes, S. Increased throughput for fragment analysis on an ABI PRISM 377 automated sequencer using a membrane comb and STRand software. Biotechniques 6, 1320–1324 (2001).
    Google Scholar 
    Belkhir, K., Castric, V. & Bonhomme, F. IDENTIX, a software to test for relatedness in a population using permutation methods. Mol. Ecol. Notes 2, 611–614 (2002).Article 

    Google Scholar 
    Queller, D. & Goodnight, K. Estimating relatedness using genetic markers. Evolution 43(2), 258–275 (1989).PubMed 
    Article 

    Google Scholar 
    Marshall, T. C., Slate, J., Kruuk, L. E. B. & Pemberton, J. M. Statistical confidence for likelihood-based paternity inference in natural populations. Mol. Ecol. 7, 639–655 (1998).CAS 
    PubMed 
    Article 

    Google Scholar 
    Ottensmann, M., Stoffel, M. A., Nichols, H. J. & Hoffman, J. I. GCalignR: An R Package for aligning gas-chromatography data for ecological and evolutionary studies. PLoS ONE 13(6), e0198311 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Morelli, T. et al. Relatedness communicated in lemur scent. Naturwissenschaften 100, 769–777 (2013).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Oksanen, J., Blanchet, F., Guillaume. F., Kindt, R., Legendre, P., Minchin, P., O’Hara, R.B., Simpson, G., Solymos, P., Stevens, M.H.H., Wagner, H. Vegan: community ecology package. R package vegan, vers. 2.2-1. (2015). More

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    Coupled abiotic-biotic cycling of nitrous oxide in tropical peatlands

    Thompson, R. L. et al. Acceleration of global N2O emissions seen from two decades of atmospheric inversion. Nat. Clim. Change 9, 993–998 (2019).CAS 
    Article 

    Google Scholar 
    Tian, H. et al. A comprehensive quantification of global nitrous oxide sources and sinks. Nature 586, 248–256 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Zhuang, Q., Lu, Y. & Chen, M. An inventory of global N2O emissions from the soils of natural terrestrial ecosystems. Atm. Environ. 47, 66–75 (2012).CAS 
    Article 

    Google Scholar 
    Huang, J. et al. Estimation of regional emissions of nitrous oxide from 1997 to 2005 using multinetwork measurements, a chemical transport model, and an inverse method. J. Geophys. Res. 113, D17313 (2008).Article 

    Google Scholar 
    D’Amelio, M. T. S., Gatti, L. V., Miller, J. B. & Tans, P. Regional N2O fluxes in Amazonia derived from aircraft vertical profiles. Atmos. Chem. Phys. 9, 8785–8797 (2009).Article 

    Google Scholar 
    Teh, Y. A., Murphy, W. A., Berrio, J.-C., Boom, A. & Page, S. E. Seasonal variability in methane and nitrous oxide fluxes from tropical peatlands in the western Amazon basin. Biogeosciences 14, 3669–3683 (2017).CAS 
    Article 

    Google Scholar 
    Finn, D. R. et al. Methanogens and methanotrophs show nutrient-dependent community assemblage patterns across tropical peatlands of the Pastaza-Marañón Basin, Peruvian Amazonia. Front. Microbiol. 11, 746 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Buessecker, S. et al. Effects of sterilization techniques on chemodenitrification and N2O production in tropical peat soil microcosms. Biogeosciences 16, 4601–4612 (2019).CAS 
    Article 

    Google Scholar 
    Heil, J., Liu, S., Vereecken, H. & Brüggemann, N. Abiotic nitrous oxide production from hydroxylamine in soils and their dependence on soil properties. Soil Biol. Biochem. 84, 107–115 (2015).CAS 
    Article 

    Google Scholar 
    Samarkin, V. A. et al. Abiotic nitrous oxide emission from the hypersaline Don Juan Pond in Antarctica. Nat. Geosci. 3, 341–344 (2010).CAS 
    Article 

    Google Scholar 
    Otte, J. M. et al. N2O formation by nitrite-induced (chemo)denitrification in coastal marine sediment. Sci. Rep. 9, 10691 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Jones, L. C., Peters, B., Pacheco, J. S. L., Casciotti, K. L. & Fendorf, S. Stable isotopes and iron oxide mineral products as markers of chemodenitrification. Environ. Sci. Technol. 49, 3444–3452 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Tolman, W. B. Binding and activation of N2O at transition-metal centers: recent mechanistic insights. Angew. Chem. Int. Ed. 49, 1018–1024 (2010).CAS 
    Article 

    Google Scholar 
    Holtan-Hartwig, L., Dörsch, P. & Bakken, L. R. Low temperature control of soil denitrifying communities: kinetics of N2O production and reduction. Soil Biol. Biochem. 34, 1797–1806 (2002).CAS 
    Article 

    Google Scholar 
    Gorelsky, S. I., Ghosh, S. & Solomon, E. I. Mechanism of N2O reduction by the μ4-S tetranuclear CuZ cluster of nitrous oxide reductase. J. Am. Chem. Soc. https://doi.org/10.1021/ja055856o (2005).Tsai, M.-L. et al. [Cu2O]2+ active site formation in Cu–ZSM-5: geometric and electronic structure requirements for N2O activation. J. Am. Chem. Soc. https://doi.org/10.1021/ja4113808 (2014).Sanford, R. A. et al. Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils. Proc. Natl Acad. Sci. USA 109, 19709–19714 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Jones, C. M. et al. Recently identified microbial guild mediates soil N2O sink capacity. Nat. Clim. Change 4, 801–805 (2014).CAS 
    Article 

    Google Scholar 
    Hallin, S., Philippot, L., Löffler, F. E., Sanford, R. A. & Jones, C. M. Genomics and ecology of novel N2O-reducing microorganisms. Trends Microbiol. 26, 43–55 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Lycus, P. et al. A bet-hedging strategy for denitrifying bacteria curtails their release of N2O. Proc. Natl Acad. Sci. USA 115, 11820–11825 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Burns, L. C., Stevens, R. J. & Laughlin, R. J. Determination of the simultaneous production and consumption of soil nitrite using 15N. Soil Biol. Biochem. 27, 839–844 (1995).CAS 
    Article 

    Google Scholar 
    Burns, L. C., Stevens, R. J. & Laughlin, R. J. Production of nitrite in soil by simultaneous nitrification and denitrification. Soil Biol. Biochem. 28, 609–616 (1996).CAS 
    Article 

    Google Scholar 
    Wullstein, L. H. & Gilmour, C. M. Non-enzymatic formation of nitrogen gas. Nature 210, 1150–1151 (1966).CAS 
    Article 

    Google Scholar 
    Liu, S., Schloter, M., Hu, R., Vereecken, H. & Brüggemann, N. Hydroxylamine contributes more to abiotic N2O production in soils than nitrite. Front. Environ. Sci. https://doi.org/10.3389/fenvs.2019.00047 (2019).Thorn, K. A. & Mikita, M. A. Nitrite fixation by humic substances: nitrogen-15 nuclear magnetic resonance evidence for potential intermediates in chemodenitrification. Soil Sci. Soc. Am. J. 64, 568–582 (2000).CAS 
    Article 

    Google Scholar 
    Thorn, K. A., Younger, S. J. & Cox, L. G. Order of functionality loss during photodegradation of aquatic humic substances. J. Environ. Qual. 39, 1416–1428 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    Klüpfel, L., Piepenbrock, A., Kappler, A. & Sander, M. Humic substances as fully regenerable electron acceptors in recurrently anoxic environments. Nat. Geosci. 7, 195–200 (2014).Article 

    Google Scholar 
    Lovley, D. R. & Blunt-Harris, E. L. Role of humic-bound iron as an electron transfer agent in dissimilatory Fe(III) reduction. Appl. Environ. Microbiol. 65, 4252–4254 (1999).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kappler, A., Benz, M., Schink, B. & Brune, A. Electron shuttling via humic acids in microbial iron(III) reduction in a freshwater sediment. FEMS Microbiol. Ecol. 47, 85–92 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    Van Cleemput, O., Patrick, W. H. & McIlhenny, R. C. Nitrite decomposition in flooded soil under different pH and redox potential conditions. Soil Sci. Soc. Am. J. 40, 55–60 (1976).Article 

    Google Scholar 
    Van Cleemput, O. & Baert, L. Nitrite: a key compound in N loss processes under acid conditions? Plant Soil 76, 233–241 (1984).Article 

    Google Scholar 
    Porter, L. K. Gaseous products produced by anaerobic reaction of sodium nitrite with oxime compounds and oximes synthesized from organic matter. Soil Sci. Soc. Am. J. 33, 696–702 (1969).CAS 
    Article 

    Google Scholar 
    Liu, B., Mørkved, P. T., Frostegård, Å. & Bakken, L. R. Denitrification gene pools, transcription and kinetics of NO, N2O and N2 production as affected by soil pH. FEMS Microbiol. Ecol. 72, 407–417 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    Palmer, K., Biasi, C. & Horn, M. A. Contrasting denitrifier communities relate to contrasting N2O emission patterns from acidic peat soils in arctic tundra. ISME J. 6, 1058–1077 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Domeignoz-Horta, L. et al. The diversity of the N2O reducers matters for the N2O:N2 denitrification end-product ratio across an annual and a perennial cropping system. Front. Microbiol. https://doi.org/10.3389/fmicb.2015.00971 (2015).Domeignoz-Horta, L. A. et al. Peaks of in situ N2O emissions are influenced by N2O-producing and reducing microbial communities across arable soils. Glob. Change Biol. 24, 360–370 (2018).Article 

    Google Scholar 
    Onley, J. R., Ahsan, S., Sanford, R. A. & Löffler, F. E. Denitrification by Anaeromyxobacter dehalogenans, a common soil bacterium lacking the nitrite reductase genes nirS and nirK. Appl. Environ. Microbiol. 84, 4 (2018).Article 

    Google Scholar 
    Sanford, R. A., Cole, J. R. & Tiedje, J. M. Characterization and description of Anaeromyxobacter dehalogenans gen. nov., sp. nov., an aryl-halorespiring facultative anaerobic myxobacterium. Appl. Environ. Microbiol. 68, 893–900 (2002).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Mohr, K. I., Zindler, T., Wink, J., Wilharm, E. & Stadler, M. Myxobacteria in high moor and fen: an astonishing diversity in a neglected extreme habitat. MicrobiologyOpen 6, e00464 (2017).PubMed Central 
    Article 

    Google Scholar 
    Hori, T., Müller, A., Igarashi, Y., Conrad, R. & Friedrich, M. W. Identification of iron-reducing microorganisms in anoxic rice paddy soil by ¹³C-acetate probing. ISME J. 4, 267–278 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    Kawaichi, S. et al. Ardenticatena maritima gen. nov., sp. nov., a ferric iron- and nitrate-reducing bacterium of the phylum ‘Chloroflexi’ isolated from an iron-rich coastal hydrothermal field, and description of Ardenticatenia classis nov. Int. J. Sys. Evol. Microbiol. 63, 2992–3002 (2013).CAS 
    Article 

    Google Scholar 
    Podosokorskaya, O. A. et al. Characterization of Melioribacter roseus gen. nov., sp. nov., a novel facultatively anaerobic thermophilic cellulolytic bacterium from the class Ignavibacteria, and a proposal of a novel bacterial phylum Ignavibacteriae. Environ. Microbiol. 15, 1759–1771 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Yoon, S. et al. Nitrous oxide reduction kinetics distinguish bacteria harboring clade I nosz from those harboring clade II NosZ. Appl. Environ. Microbiol. 82, 3793–3800 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Maher, B. A. & Taylor, R. M. Formation of ultrafine-grained magnetite in soils. Nature 336, 368–370 (1988).CAS 
    Article 

    Google Scholar 
    Sanchez, P. A. Properties and Management of Soils in the Tropics (Wiley, 1976).White, A. F. et al. Chemical weathering in a tropical watershed, Luquillo Mountains, Puerto Rico: I. Long-term versus short-term weathering fluxes. Geochim. Cosmochim. Acta 62, 209–226 (1998).CAS 
    Article 

    Google Scholar 
    Hall, S. J., Liptzin, D., Buss, H. L., DeAngelis, K. & Silver, W. L. Drivers and patterns of iron redox cycling from surface to bedrock in a deep tropical forest soil: a new conceptual model. Biogeochemistry 130, 177–190 (2016).CAS 
    Article 

    Google Scholar 
    Buchwald, C., Grabb, K., Hansel, C. M. & Wankel, S. D. Constraining the role of iron in environmental nitrogen transformations: dual stable isotope systematics of abiotic NO2− reduction by Fe(II) and its production of N2O. Geochim. Cosmochim. Acta 186, 1–12 (2016).CAS 
    Article 

    Google Scholar 
    Grabb, K. C., Buchwald, C., Hansel, C. M. & Wankel, S. D. A dual nitrite isotopic investigation of chemodenitrification by mineral-associated Fe(II) and its production of nitrous oxide. Geochim. Cosmochim. Acta 196, 388–402 (2017).CAS 
    Article 

    Google Scholar 
    Drewer, J. et al. Linking nitrous oxide and nitric oxide fluxes to microbial communities in tropical forest soils and oil palm plantations in Malaysia in laboratory incubations. Front. For. Glob. Change 3, 4 (2020).Article 

    Google Scholar 
    Yvon-Durocher, G., Jones, J. I., Trimmer, M., Woodward, G. & Montoya, J. M. Warming alters the metabolic balance of ecosystems. Phil. Trans. R. Soc. B 365, 2117–2126 (2010).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Yvon-Durocher, G. et al. Reconciling the temperature dependence of respiration across timescales and ecosystem types. Nature 487, 472–476 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Jauhiainen, J., Kerojoki, O., Silvennoinen, H., Limin, S. & Vasander, H. Heterotrophic respiration in drained tropical peat is greatly affected by temperature – a passive ecosystem cooling experiment. Environ. Res. Lett. 9, 105013 (2014).Article 

    Google Scholar 
    Wang, S., Zhuang, Q., Lähteenoja, O., Draper, F. C. & Cadillo-Quiroz, H. Potential shift from a carbon sink to a source in Amazonian peatlands under a changing climate. Proc. Natl Acad. Sci. USA 115, 12407–12412 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Stumm, W. & Lee, G. F. Oxygenation of ferrous iron. Ind. Eng. Chem. 53, 143–146 (1961).CAS 
    Article 

    Google Scholar 
    Theis, T. L. & Singer, P. C. Complexation of iron(II) by organic matter and its effect on iron(II) oxygenation. Environ. Sci. Technol. 8, 569–573 (1974).CAS 
    Article 

    Google Scholar 
    Wan, X. et al. Complexation and reduction of iron by phenolic substances: implications for transport of dissolved Fe from peatlands to aquatic ecosystems and global iron cycling. Chem. Geol. 498, 128–138 (2018).CAS 
    Article 

    Google Scholar 
    Daugherty, E. E., Gilbert, B., Nico, P. S. & Borch, T. Complexation and redox buffering of iron(II) by dissolved organic matter. Environ. Sci. Technol. 51, 11096–11104 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Prananto, J. A., Minasny, B., Comeau, L.-P., Rudiyanto, R. & Grace, P. Drainage increases CO2 and N2O emissions from tropical peat soils. Glob. Change Biol. 26, 4583–4600 (2020).Article 

    Google Scholar 
    Stirling, E., Fitzpatrick, R. W. & Mosley, L. Drought effects on wet soils in inland wetlands and peatlands. Earth Sci. Rev. 210, 103387 (2020).CAS 
    Article 

    Google Scholar 
    Hodgkins, S. B. et al. Tropical peatland carbon storage linked to global latitudinal trends in peat recalcitrance. Nat. Commun. 9, 3640 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Gumbricht, T. et al. An expert system model for mapping tropical wetlands and peatlands reveals South America as the largest contributor. Glob. Change Biol. 23, 3581–3599 (2017).Article 

    Google Scholar 
    IPCC Climate Change 2021: The Physical Science Basis (eds Masson-Delmotte, V. et al.) (Cambridge Univ. Press, 2021).Babbin, A. R., Bianchi, D., Jayakumar, A. & Ward, B. B. Rapid nitrous oxide cycling in the suboxic ocean. Science 348, 1127–1129 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hamilton, S. K. & Ostrom, N. E. Measurement of the stable isotope ratio of dissolved N2 in 15N tracer experiments. Limnol. Oceanogr. Methods 5, 233–240 (2007).CAS 
    Article 

    Google Scholar 
    Ostrom, N. E., Gandhi, H., Trubl, G. & Murray, A. E. Chemodenitrification in the cryoecosystem of Lake Vida, Victoria Valley, Antarctica. Geobiology 14, 575–587 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Stumm, W. & Morgan, J. J. Aquatic Chemistry 3rd edn (John Wiley & Sons, 1996).Homyak, P. M., Kamiyama, M., Sickman, J. O. & Schimel, J. P. Acidity and organic matter promote abiotic nitric oxide production in drying soils. Glob. Change Biol. 23, 1735–1747 (2017).Article 

    Google Scholar 
    Henry, S., Bru, D., Stres, B., Hallet, S. & Philippot, L. Quantitative detection of the nosZ gene, encoding nitrous oxide reductase, and comparison of the abundances of 16S rRNA, narG, nirK, and nosZ genes in soils. Appl. Environ. Microbiol. 72, 5181–5189 (2006).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Jones, C. M., Graf, D. R., Bru, D., Philippot, L. & Hallin, S. The unaccounted yet abundant nitrous oxide-reducing microbial community: a potential nitrous oxide sink. ISME J. 7, 417–426 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Zhang, B. et al. A new primer set for clade I nosZ that recovers genes from a broader range of taxa. Biol. Fertil. Soils 57, 523–531 (2021).CAS 
    Article 

    Google Scholar 
    Herbold, C. W. et al. A flexible and economical barcoding approach for highly multiplexed amplicon sequencing of diverse target genes. Front. Microbiol. 6, 8966 (2015).Article 

    Google Scholar 
    Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    Edgar, R. C. UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing. Preprint at https://www.biorxiv.org/content/early/2016/10/15/081257 (2016).Wang, Q. et al. Ecological patterns of nifH genes in four terrestrial climatic zones explored with targeted metagenomics using Framebot, a new informatics tool. mBio 4, e00592-13 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Buchfink, B., Xie, C. & Huson, D. H. Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12, 59–60 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Fish, J. A. et al. FunGene: the functional gene pipeline and repository. Front. Microbiol. 4, 291 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Huson, D. H. et al. MEGAN Community Edition – interactive exploration and analysis of large-scale microbiome sequencing data. PLoS Comput. Biol. 12, e1004957 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Huson, D. H. et al. MEGAN-LR: new algorithms allow accurate binning and easy interactive exploration of metagenomic long reads and contigs. Biol. Direct 13, 6 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ondov, B. D., Bergman, N. H. & Phillippy, A. M. Interactive metagenomic visualization in a Web browser. BMC Bioinformatics 12, 385 (2011).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar  More