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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

    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

  • in

    Connectivity modelling in conservation science: a comparative evaluation

    Abram, D. The spell of the sensuous: Perception and language in a more-than-human world. Vintage (2012).Ingold, T. Being alive: Essays on movement, knowledge and description. Routledgehttps://doi.org/10.4324/9780203818336 (2011).Article 

    Google Scholar 
    Kimmerer, R.W. Braiding sweetgrass: Indigenous wisdom, scientific knowledge and the teachings of plants (Milkweed editions, 2013).Tucker, M. A. et al. Moving in the Anthropocene: Global reductions in terrestrial mammalian movements. Science 359(6374), 466–469 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    Gibbs, J.P. Amphibian movements in response to forest edges, roads, and streambeds in southern New England. in The Journal of Wildlife Management (1998), pp. 584–589. https://doi.org/10.2307/3802333.Moller, H., Berkes, F., O’Brian Lyver, P., & Kislalioglu, M. Combining science and traditional ecological knowledge: Monitoring populations for co-management. in Ecology and society (2004).Lorimer, J. Wildlife in the Anthropocene: conservation after nature. (U of Minnesota Press, 2015).Wiens, J. A. Spatial scaling in ecology. Funct. Ecol. 3(4), 385–397 (1989).Article 

    Google Scholar 
    Abram, D. Becoming animal: An earthly cosmology. Vintage (2010).Nathan, R. et al. A movement ecology paradigm for unifying organismal movement research. Proc. Natl. Acad. Sci. 105(49), 19052–19059 (2008).ADS 
    CAS 
    Article 

    Google Scholar 
    Tischendorf, L. & Fahrig, L. On the usage and measurement of landscape connectivity. Oikos 90(1), 7–19. https://doi.org/10.1034/j.1600-0706.2000.900102.x (2000).Article 

    Google Scholar 
    Rudnick, D., Ryan, S.J., Beier, P., Cushman, S.A., Dieffenbach, F., Epps, C., Gerber, L.R., Hartter, J.N., Jenness, J.S., & Kintsch, J. et al. The role of landscape connectivity in planning and implementing conservation and restoration priorities. Issues in Ecology (2012).Hilty, J.A., Lidicker, W.Z., & Merenlender, A.M. Corridor Ecology: The Science and Practice of Linking Landscapes for Biodiversity Conservation (Island Press, 2012).Cushman, S.A., McRae, B.H., Adriaensen, F., Beier, P., Shirley, M., & Zeller, K. Biological corridors and connectivity [Chapter 21]. in Key Topics in Conservation Biology 2nd ed. (eds Macdonald, D.W., Willis, K.J.) pp. 384–404 (Hoboken, NJ: Wiley-Blackwell, 2013).Unnithan Kumar, S., Turnbull, J., Hartman Davies, O., Hodgetts, T., & Cushman, S.A. Moving beyond landscape resistance: Considerations for the future of connectivity modelling and conservation science. in Landscape Ecology (2022).Zeller, K. A., McGarigal, K. & Whiteley, A. R. Estimating landscape resistance to movement: a review. Landscape Ecol. 27(6), 777–797 (2012).Article 

    Google Scholar 
    Adriaensen, F. et al. The application of ‘least-cost’ modelling as a functional landscape model. Landsc. Urban Plan. 64(4), 233–247 (2003).Article 

    Google Scholar 
    Cushman, S. A. & McKelvey, K. S. Use of empirically derived source-destination models to map regional conservation corridors. Conserv. Biol. 23(2), 368–376. https://doi.org/10.1111/j.1523-1739.2008.01111.x (2009).Article 
    PubMed 

    Google Scholar 
    Moilanen, A. On the limitations of graph-theoretic connectivity in spatial ecology and conservation. J. Appl. Ecol. pp. 1543–1547 (2011).Compton, B. W., McGarigal, K., Cushman, S. A. & Gamble, L. R. A resistant kernel model of connectivity for amphibians that breed in vernal pools. Conserv. Biol. 21(3), 788–799. https://doi.org/10.1111/j.1523-1739.2007.00674.x (2007).Article 
    PubMed 

    Google Scholar 
    McRae, B. H., Dickson, B. G., Keitt, T. H. & Shah, V. B. Using circuit theory to model connectivity in ecology, evolution, and conservation. Ecology 89(10), 2712–2724. https://doi.org/10.1890/07-1861.1. (2008).Article 
    PubMed 

    Google Scholar 
    Zeller, K. A. et al. Are all data types and connectivity models created equal? Validating common connectivity approaches with dispersal data. Divers. Distrib. 24(7), 868–879. https://doi.org/10.1111/ddi.12742. (2018).Article 

    Google Scholar 
    Pullinger, M. G. & Johnson, C. J. Maintaining or restoring connectivity of modified landscapes: evaluating the least-cost path model with multiple sources of ecological information. Landscape Ecol. 25(10), 1547–1560 (2010).Article 

    Google Scholar 
    Sawyer, S. C., Clinton, W. E. & Brashares, J. S. Placing linkages among fragmented habitats: do least-cost models reflect how animals use landscapes?. J. Appl. Ecol. 48(3), 668–678 (2011).Article 

    Google Scholar 
    Laliberté, J. & St-Laurent, M.-H. Validation of functional connectivity modeling: The Achilles’ heel of landscape connectivity mapping. Landsc. Urban Plan. 202, 103878 (2020).Article 

    Google Scholar 
    Landguth, E. L. & Cushman, S. A. CDPOP: A spatially explicit cost distance popula tion genetics program. Mol. Ecol. Resour. 10(1), 156–161. https://doi.org/10.1111/j.1755-0998.2009.02719.x. (2010).CAS 
    Article 
    PubMed 

    Google Scholar 
    Landguth, E. L. et al. Quantifying the lag time to detect barriers in landscape genetics. Mol. Ecol. 19(19), 4179–4191. https://doi.org/10.1111/j.1365-294X.2010.04808.x (2010).CAS 
    Article 
    PubMed 

    Google Scholar 
    Cushman, S. A. & Landguth, E. L. Scale dependent inference in landscape genetics. Landsc. Ecol. 25(6), 967–979 (2010).Article 

    Google Scholar 
    Cushman, S. A., Shirk, A. J. & Landguth, E. L. Separating the effects of habitat area, fragmentation and matrix resistance on genetic differentiation in complex landscapes. Landscape Ecol. 27(3), 369–380. https://doi.org/10.1007/s10980-011-9693-0 (2012).Article 

    Google Scholar 
    Macdonald, E. A. et al. Simulating impacts of rapid forest loss on population size, connectivity and genetic diversity of Sunda clouded leopards (Neofelis diardi) in Borneo. PLoS ONE 13(9), e0196974 (2018).Article 

    Google Scholar 
    Schumaker, N. H. et al. Mapping sources, sinks, and connectivity using a simulation model of northern spotted owls. Landscape Ecol. 29(4), 579–592 (2014).Article 

    Google Scholar 
    Unnithan Kumar, S., Kaszta, Ż & Cushman, S. A. Pathwalker: A new individual-based movement model for conservation science and connectivity modelling. ISPRS Int. J. Geo Inf. 11(6), 329 (2022).Article 

    Google Scholar 
    Virtanen, P. et al. SciPy 1.0: Fundamental algorithms for scientific computing in Python. Nat. Methods 17(3), 261–272 (2020).CAS 
    Article 

    Google Scholar 
    Dixon, P. VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14(6), 927–930 (2003).Article 

    Google Scholar 
    Dray, S., Royer-Carenzi, M. & Calenge, C. The exploratory analysis of autocorrelation in animal-movement studies. Ecol. Res. 25(3), 673–681. https://doi.org/10.1007/s11284-010-0701-7 (2010).Article 

    Google Scholar 
    Cushman, S.A. Animal movement data: GPS telemetry, autocorrelation and the need for path-level analysis. in Spatial Complexity, Informatics, and Wildlife Conservation (Springer, 2010), pp. 131-149.Zeller, K. A. et al. Sensitivity of landscape resistance estimates based on point selection functions to scale and behavioral state: pumas as a case study. Landscape Ecol. 29(3), 541–557 (2014).Article 

    Google Scholar 
    Kareiva, P. M. & Shigesada, N. Analyzing insect movement as a correlated random walk. Oecologia 56(2), 234–238 (1983).ADS 
    CAS 
    Article 

    Google Scholar 
    Schumaker, N.H. Using landscape indices to predict habitat connectivity. Ecology (1996), pp. 1210–1225.Schumaker, N. H. & Brookes, A. HexSim: A modeling environment for ecology and conservation. Landscape Ecol. 33(2), 197–211 (2018).Article 

    Google Scholar 
    Bocedi, G., Palmer, S. C. F., Malchow, A.-K., Zurell, D. & Watts, K. RangeShifter 2.0: An extended and enhanced platform for modelling spatial eco-evolutionary dynamics and species’ responses to environmental changes. Ecography 44(10), 1453–1462 (2021).Article 

    Google Scholar 
    Kaszta, Ż, Cushman, S. A. & Slotow, R. Temporal non-stationarity of path- selection movement models and connectivity: An example of African elephants in Kruger national park. Front. Ecol. Evol. 9, 207 (2021).Article 

    Google Scholar 
    Osipova, L. et al. Using step-selection functions to model landscape connectivity for African elephants: Accounting for variability across individuals and seasons. Anim. Conserv. 22(1), 35–48 (2019).Article 

    Google Scholar 
    Vergara, M., Cushman, S. A. & Ruiz-González, A. Ecological differences and limiting factors in different regional contexts: landscape genetics of the stone marten in the Iberian Peninsula. Landscape Ecol. 32(6), 1269–1283 (2017).Article 

    Google Scholar 
    Reddy, P. A., Puyravaud, J.-P., Cushman, S. A. & Segu, H. Spatial variation in the response of tiger gene ow to landscape features and limiting factors. Anim. Conserv. 22(5), 472–480 (2019).Article 

    Google Scholar 
    Zeller, K. A., Lewsion, R., Fletcher, R. J., Tulbure, M. G. & Jennings, M. K. Understanding the importance of dynamic landscape connectivity. Land 9(9), 303. https://doi.org/10.3390/land9090303 (2020).Article 

    Google Scholar 
    Cronon, W. The trouble with wilderness: or, getting back to the wrong nature. Environ. Hist. 1(1), 7–28 (1996).Article 

    Google Scholar 
    Ingold, T. The Perception of the Environment: Essays on Livelihood, Dwelling and Skill (Routledge, 2021).Boettiger, A. N. et al. Inferring ecological and behavioral drivers of African elephant movement using a linear filtering approach. Ecology 92(8), 1648–1657 (2011).Article 

    Google Scholar 
    Pooley, S. et al. An interdisciplinary review of current and future approaches to improving human-predator relations. Conserv. Biol. 31(3), 513–523. https://doi.org/10.1111/cobi.12859 (2017).CAS 
    Article 
    PubMed 

    Google Scholar 
    Benson, E. S. Minimal animal: Surveillance, simulation, and stochasticity in wildlife biology. Antennae 30, 39 (2014).
    Google Scholar 
    Kaszta, Ż et al. Integrating Sunda clouded leopard (Neofelis diardi) conservation into development and restoration planning in Sabah (Borneo). Biol. Cons. 235, 63–76 (2019).Article 

    Google Scholar 
    Penjor, U., Astaras, C., Cushman, S. A., Kaszta, Ż & Macdonald, D. W. Contrasting effects of human settlement on the interaction among sympatric apex carnivores. Proc. R. Soc. B 289(1973), 20212681 (2022).Article 

    Google Scholar 
    Barua, M. Bio-geo-graphy: Landscape, dwelling, and the political ecology of human-elephant relations. Environ. Plann. D Soc. Space 32(5), 915–934 (2014).Article 

    Google Scholar 
    Elliot, N. B., Cushman, S. A., Macdonald, D. W. & Loveridge, A. J. The devil is in the dispersers: Predictions of landscape connectivity change with demography. J. Appl. Ecol. 51(5), 1169–1178 (2014).Article 

    Google Scholar 
    Kareiva, P. & Marvier, M. What is conservation science?. Bioscience 62(11), 962–969 (2012).Article 

    Google Scholar 
    Bennett, N. J. et al. Conservation social science: Understanding and integrating human dimensions to improve conservation. Biol. Conserv. 205, 93–108 (2017).Article 

    Google Scholar 
    Bunnefeld, N., Nicholson, E., & Milner-Gulland, E.J. Decision-Making in Conservation and Natural Resource Management: Models for Interdisciplinary Approaches. (Vol. 22, Cambridge University Press, 2017).Parathian, H. E., McLennan, M. R., Hill, C. M., Fraza o-Moreira, A. & Hockings, K. J. Breaking through disciplinary barriers: Human-wildlife interactions and multispecies ethnography. Int. J. Primatol. 39(5), 749–775 (2018).Article 

    Google Scholar 
    Hodgetts, T. Connectivity as a multiple: In with and as “nature’’. Area 50(1), 83–90. https://doi.org/10.1111/area.12353 (2018).Article 
    PubMed 

    Google Scholar 
    Berkes, F. Sacred ecology (Routledge, 2017). https://doi.org/10.4324/9781315114644.Parrenas, J.S. Decolonizing Extinction: The Work of Care in Orangutan Rehabilitation (Duke University Press, 2018).Bill Adams, W., & Mulligan, M. Decolonizing Nature: Strategies for Conservation in a Post-Colonial Era (Routledge, 2012). More

  • in

    Industrial energy development decouples ungulate migration from the green wave

    Bolger, D. T., Newmark, W. D., Morrison, T. A. & Doak, D. F. The need for integrative approaches to understand and conserve migratory ungulates. Ecol. Lett. 11, 63–77 (2008).PubMed 

    Google Scholar 
    Fryxell, J. M., Greever, J. & Sinclair, A. R. E. Why are migratory ungulates so abundant. Am. Nat. 131, 781–798 (1988).Article 

    Google Scholar 
    Holdo, R. M., Holt, R. D., Sinclair, A. R., Godley, B. J. & Thirgood, S. in Animal Migration: A Synthesis (eds Milner-Gulland, E. J. et al.) 131–143 (Oxford Univ. Press, 2011).Bauer, S. & Hoye, B. J. Migratory animals couple biodiversity and ecosystem functioning worldwide. Science 344, 1242552 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    Middleton, A. D. et al. Conserving transboundary wildlife migrations: recent insights from the Greater Yellowstone Ecosystem. Front. Ecol. Environ. 18, 83–91 (2020).Article 

    Google Scholar 
    Aikens, E. O. et al. Wave-like patterns of plant phenology determine ungulate movement tactics. Curr. Biol. 30, 3444–3449 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Mueller, T. & Fagan, W. F. Search and navigation in dynamic environments—from individual behaviors to population distributions. Oikos 117, 654–664 (2008).Article 

    Google Scholar 
    Fryxell, J. M. Forage quality and aggregation by large herbivores. Am. Nat. 138, 478–498 (1991).Article 

    Google Scholar 
    Drent, R., Ebbinge, B. & Weijand, B. Balancing the energy budgets of arctic-breeding geese throughout the annual cycle: a progress report. Verh. Ornithol. Ges. Bayern 23, 239–264 (1978).
    Google Scholar 
    van der Graaf, S. A. J., Stahl, J., Klimkowska, A., Bakker, J. P. & Drent, R. H. Surfing on a green wave—how plant growth drives spring migration in the Barnacle Goose Branta leucopsis. Ardea 94, 567–577 (2006).
    Google Scholar 
    Merkle, J. A. et al. Large herbivores surf waves of green-up during spring. Proc. R. Soc. B. 283, 20160456 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Aikens, E. O. et al. The greenscape shapes surfing of resource waves in a large migratory herbivore. Ecol. Lett. 20, 741–750 (2017).PubMed 
    Article 

    Google Scholar 
    Middleton, A. D. et al. Green-wave surfing increases fat gain in a migratory ungulate. Oikos https://doi.org/10.1111/oik.05227 (2018).Jesmer, B. R. et al. Is ungulate migration culturally transmitted? Evidence of social learning from translocated animals. Science 361, 1023–1025 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Sawyer, H. et al. A framework for understanding semi‐permeable barrier effects on migratory ungulates. J. Appl. Ecol. 50, 68–78 (2013).Article 

    Google Scholar 
    Kauffman, M. J. et al. Mapping out a future for ungulate migrations. Science 372, 566–569 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Doherty, T. S., Hays, G. C. & Driscoll, D. A. Human disturbance causes widespread disruption of animal movement. Nat. Ecol. Evol. 5, 513–519 (2021).PubMed 
    Article 

    Google Scholar 
    Berry, J. Aspects of wildebeest Connochaetes taurinus ecology in the Etosha National Park—a synthesis for future management. Madoqua 1997, 137–148 (1997).
    Google Scholar 
    Williamson, D. & Williamson, J. Botswana’s fences and the depletion of Kalahari wildlife. Oryx 18, 218–222 (1984).Article 

    Google Scholar 
    Northrup, J. M. & Wittemyer, G. Characterising the impacts of emerging energy development on wildlife, with an eye towards mitigation. Ecol. Lett. 16, 112–125 (2013).PubMed 
    Article 

    Google Scholar 
    Kauffman, M. J., Meacham, J. E., Sawyer, H., Rudd, W. & Ostlind, E. Wild Migrations: Atlas of Wyoming’s Ungulates (Oregon State Univ. Press, 2018).Wyckoff, T. B., Sawyer, H., Albeke, S. E., Garman, S. L. & Kauffman, M. J. Evaluating the influence of energy and residential development on the migratory behavior of mule deer. Ecosphere 9, e02113 (2018).Article 

    Google Scholar 
    Lendrum, P. E., Anderson, C. R. Jr., Monteith, K. L., Jenks, J. A. & Bowyer, R. T. Migrating mule deer: effects of anthropogenically altered landscapes. PLoS ONE 8, e64548 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lendrum, P. E., Anderson, C. R. Jr, Long, R. A., Kie, J. G. & Bowyer, R. T. Habitat selection by mule deer during migration: effects of landscape structure and natural‐gas development. Ecosphere 3, 82 (2012).Sawyer, H. & Kauffman, M. J. Stopover ecology of a migratory ungulate. J. Anim. Ecol. 80, 1078–1087 (2011).PubMed 
    Article 

    Google Scholar 
    Sawyer, H., LeBeau, C. W., McDonald, T. L., Xu, W. & Middleton, A. D. All routes are not created equal: an ungulate’s choice of migration route can influence its survival. J. Appl. Ecol. 56, 1860–1869 (2019).
    Google Scholar 
    Bischof, R. et al. A migratory northern ungulate in the pursuit of spring: jumping or surfing the green wave? Am. Nat. 180, 407–424 (2012).PubMed 
    Article 

    Google Scholar 
    Skarin, A., Nellemann, C., Rönnegård, L., Sandström, P. & Lundqvist, H. Wind farm construction impacts reindeer migration and movement corridors. Landsc. Ecol. 30, 1527–1540 (2015).Article 

    Google Scholar 
    Mysterud, A., Langvatn, R., Yoccoz, N. G. & Stenseth, N. C. Plant phenology, migration and geographical variation in body weight of a large herbivore: the effect of a variable topography. J. Anim. Ecol. 70, 915–923 (2001).Article 

    Google Scholar 
    Johnson, H. E. et al. Increases in residential and energy development are associated with reductions in recruitment for a large ungulate. Glob. Change Biol. 23, 578–591 (2017).Article 

    Google Scholar 
    Sawyer, H., Korfanta, N. M., Nielson, R. M., Monteith, K. L. & Strickland, D. Mule deer and energy development—long-term trends of habituation and abundance. Glob. Change Biol. 23, 4521–4529 (2017).Article 

    Google Scholar 
    Sawyer, H., Lambert, M. S. & Merkle, J. A. Migratory disturbance thresholds with mule deer and energy development. J. Wildl. Manag. 84, 930–937 (2020).Article 

    Google Scholar 
    Uezu, A., Metzger, J. P. & Vielliard, J. M. E. Effects of structural and functional connectivity and patch size on the abundance of seven Atlantic Forest bird species. Biol. Conserv. 123, 507–519 (2005).Article 

    Google Scholar 
    Keeley, A. T. H., Beier, P. & Jenness, J. S. Connectivity metrics for conservation planning and monitoring. Biol. Conserv. 255, 109008 (2021).Article 

    Google Scholar 
    Abrahms, B. et al. Emerging perspectives on resource tracking and animal movement ecology. Trends Ecol. Evol. 36, 308–320 (2021).PubMed 
    Article 

    Google Scholar 
    Aikens, E. O. et al. Migration distance and maternal resource allocation determine timing of birth in a large herbivore. Ecology 102, e03334 (2021).PubMed 
    Article 

    Google Scholar 
    Aikens, E. O. et al. Drought reshuffles plant phenology and reduces the foraging benefit of green-wave surfing for a migratory ungulate. Glob. Change Biol. 26, 4215–4225 (2020).Article 

    Google Scholar 
    Sawyer, H., Merkle, J. A., Middleton, A. D., Dwinnell, S. P. H. & Monteith, K. L. Migratory plasticity is not ubiquitous among large herbivores. J. Anim. Ecol. 88, 450–460 (2019).PubMed 

    Google Scholar 
    Schlaepfer, M. A., Runge, M. C. & Sherman, P. W. Ecological and evolutionary traps. Trends Ecol. Evol. 17, 474–480 (2002).Article 

    Google Scholar 
    Delibes, M., Gaona, P. & Ferreras, P. Effects of an attractive sink leading into maladaptive habitat selection. Am. Nat. 158, 277–285 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    Sawyer, H., Kauffman, M. J., Nielson, R. M. & Horne, J. S. Identifying and prioritizing ungulate migration routes for landscape-level conservation. Ecol. Appl. 19, 2016–2025 (2009).PubMed 
    Article 

    Google Scholar 
    Sawyer, H., Hayes, M., Rudd, B. & Kauffman, M. J. The Red Desert to Hoback Mule Deer Migration Assessment (Univ. Wyoming, 2014).Berger, J., Young, J. K. & Berger, K. M. Protecting migration corridors: challenges and optimism for Mongolian saiga. PLoS Biol. 6, e165 (2008).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Sikes, R. S. & Gannon, W. L. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J. Mammal. 92, 235–253 (2011).Article 

    Google Scholar 
    Vermote, E. MOD09A1 Surface Reflectance 8-day L3 Global 500m SIN Grid V006 (NASA EOSDIS Land Processes DAAC, 2015).Pettorelli, N., Mysterud, A., Yoccoz, N. G., Langvatn, R. & Stenseth, N. C. Importance of climatological downscaling and plant phenology for red deer in heterogeneous landscapes. Proc. R. Soc. B. 272, 2357–2364 (2005).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Pettorelli, N. et al. Using the satellite-derived NDVI to assess ecological responses to environmental change. Trends Ecol. Evol. 20, 503–510 (2005).PubMed 
    Article 

    Google Scholar 
    Hamel, S., Garel, M., Festa-Bianchet, M., Gaillard, J. M. & Cote, S. D. Spring normalized difference vegetation index (NDVI) predicts annual variation in timing of peak faecal crude protein in mountain ungulates. J. Appl. Ecol. 46, 582–589 (2009).Article 

    Google Scholar 
    Geremia, C. et al. Migrating bison engineer the green wave. Proc. Natl Acad. Sci. USA 116, 25707–25713 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

  • in

    Single-cell view of deep-sea microbial activity and intracommunity heterogeneity

    Orcutt BN, Sylvan JB, Knab NJ, Edwards KJ. Microbial ecology of the dark ocean above, at, and below the seafloor. Microbiol Mol Biol Rev. 2011;75:361–422.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Whitman WB, Coleman DC, Wiebe WJ. Prokaryotes: the unseen majority. Proc Natl Acad Sci USA. 1998;95:6578–83.CAS 
    PubMed 
    PubMed Central 
    Article 

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

    Google Scholar 
    Ebrahimi A, Schwartzman J, Cordero OX. Cooperation and spatial self-organization determine rate and efficiency of particulate organic matter degradation in marine bacteria. Proc Natl Acad Sci USA. 2019;116:23309–16.CAS 
    PubMed 
    PubMed Central 
    Article 

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

    Google Scholar 
    Simon M, Grossart HP, Schweitzer B, Ploug H. Microbial ecology of organic aggregates in aquatic ecosystems. Aquat Microb Ecol. 2002;28:175–211.Article 

    Google Scholar 
    Alldredge AL, Silver MW. Characteristics, dynamics and significance of marine snow. Progr Oceanogr. 1988;20:41–82.Article 

    Google Scholar 
    Zehr JP, Kudela RM. Nitrogen cycle of the open ocean: from genes to ecosystems. Ann Rev Mar Sci. 2011;3:197–225.PubMed 
    Article 

    Google Scholar 
    Bergauer K, Fernandez-Guerra A, Garcia JAL, Sprenger RR, Stepanauskas R, Pachiadaki MG, et al. Organic matter processing by microbial communities throughout the Atlantic water column as revealed by metaproteomics. Proc Natl Acad Sci USA. 2018;115:E400–8.CAS 
    PubMed 
    Article 

    Google Scholar 
    Acinas SG, Sánchez P, Salazar G, Cornejo-Castillo FM, Sebastián M, Logares R, et al. Deep ocean metagenomes provide insight into the metabolic architecture of bathypelagic microbial communities. Commun Biol. 2021;4:604.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Teira E, Lebaron P, van Aken H, Herndl GJ. Distribution and activity of Bacteria and Archaea in the deep water masses of the North Atlantic. Limnol Oceanogr. 2006;51:2131–44.CAS 
    Article 

    Google Scholar 
    Herndl GJ, Reinthaler T, Teira E, van Aken H, Veth C, Pernthaler A, et al. Contribution of Archaea to total prokaryotic production in the deep Atlantic Ocean. Appl Environ Microbiol. 2005;71:2303–9.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Gasol JM, Alonso-Sáez L, Vaqué D, Baltar F, Calleja ML, Duarte CM, et al. Mesopelagic prokaryotic bulk and single-cell heterotrophic activity and community composition in the NW Africa-Canary Islands coastal-transition zone. Progr Oceanogr. 2009;83:189–96.Article 

    Google Scholar 
    Dekas AE, Parada AE, Mayali X, Fuhrman JA, Wollard J, Weber PK, et al. Characterizing chemoautotrophy and heterotrophy in marine archaea and bacteria with single-cell multi-isotope NanoSIP. Front Microbiol. 2019;10:2682.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Musat N, Foster R, Vagner T, Adam B, Kuypers MMM. Detecting metabolic activities in single cells, with emphasis on nanoSIMS. FEMS Microbiol Rev. 2012;36:486–511.CAS 
    PubMed 
    Article 

    Google Scholar 
    Orphan VJ, House CH. Geobiological investigations using secondary ion mass spectrometry: microanalysis of extant and paleo-microbial processes. Geobiology. 2009;7:360–72.CAS 
    PubMed 
    Article 

    Google Scholar 
    Pett-Ridge J, Weber PK. NanoSIP: NanoSIMS applications for microbial biology. Methods Mol Biol. 2012;881:375–408.CAS 
    PubMed 
    Article 

    Google Scholar 
    Nuñez J, Renslow R, Cliff JB, Anderton CR. NanoSIMS for biological applications: current practices and analyses. Biointerphases. 2018;13:03B301.Article 

    Google Scholar 
    Dawson KS, Scheller S, Dillon JG, Orphan VJ. Stable isotope phenotyping via cluster analysis of NanoSIMS data as a method for characterizing distinct microbial ecophysiologies and sulfur-cycling in the environment. Front Microbiol. 2016;7:774.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Arandia-Gorostidi N, Weber PK, Alonso-Sáez L, Morán XAG, Mayali X. Elevated temperature increases carbon and nitrogen fluxes between phytoplankton and heterotrophic bacteria through physical attachment. ISME J. 2017;11:641–50.CAS 
    PubMed 
    Article 

    Google Scholar 
    Kopf SH, McGlynn SE, Green-Saxena A, Guan Y, Newman DK, Orphan VJ. Heavy water and (15) N labelling with NanoSIMS analysis reveals growth rate-dependent metabolic heterogeneity in chemostats. Environ Microbiol. 2015;17:2542–56.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Schreiber F, Littmann S, Lavik G, Escrig S, Meibom A, Kuypers MMM, et al. Phenotypic heterogeneity driven by nutrient limitation promotes growth in fluctuating environments. Nat Microbiol. 2016;1:16055.CAS 
    PubMed 
    Article 

    Google Scholar 
    Berthelot H, Duhamel S, L’Helguen S, Maguer JF, Wang S, Cetinic I, et al. NanoSIMS single cell analyses reveal the contrasting nitrogen sources for small phytoplankton. ISME J. 2019;13:651–62.CAS 
    PubMed 
    Article 

    Google Scholar 
    Calabrese F, Voloshynovska I, Musat F, Thullner M, Schlömann M, Richnow HH, et al. Quantitation and comparison of phenotypic heterogeneity among single cells of monoclonal microbial populations. Front Microbiol. 2019;10:1–23.Article 

    Google Scholar 
    Calabrese F, Stryhanyuk H, Moraru C, Schlömann M, Wick LY, Richnow HH, et al. Metabolic history and metabolic fitness as drivers of anabolic heterogeneity in isogenic microbial populations. Environ Microbiol. 2021;23:6764–76.CAS 
    PubMed 
    Article 

    Google Scholar 
    Gini C. Variabilità e Mutuabilità. Contributo allo Studio delle Distribuzioni e delle Relazioni Statistiche. C. Cuppini, Bologna; 1912.Fernández-Tschieder E, Binkley D. Linking competition with growth dominance and production ecology. Ecol Manag. 2018;414:99–107.Article 

    Google Scholar 
    Cordonnier T, Kunstler G. The Gini index brings asymmetric competition to light. Perspect Plant Ecol Evol Syst. 2015;17:107–15.Article 

    Google Scholar 
    Harch BD, Correll RL, Meech W, Kirkby CA, Pankhurst CE. Using the Gini coefficient with BIOLOG substrate utilisation data to provide an alternative quantitative measure for comparing bacterial soil communities. J Microbiol Methods. 1997;30:91–101.CAS 
    Article 

    Google Scholar 
    Li J, Ma YB, Hu HW, Wang JT, Liu YR, He JZ. Field-based evidence for consistent responses of bacterial communities to copper contamination in two contrasting agricultural soils. Front Microbiol. 2015;6:31.PubMed 
    PubMed Central 

    Google Scholar 
    Parada AE, Needham DM, Fuhrman JA. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol. 2016;18:1403–14.CAS 
    PubMed 
    Article 

    Google Scholar 
    Polerecky L, Adam B, Milucka J, Musat N, Vagner T, Kuypers MM. Look@NanoSIMS-a tool for the analysis of nanoSIMS data in environmental microbiology. Environ Microbiol. 2012;14:1009–23.CAS 
    PubMed 
    Article 

    Google Scholar 
    Stryhanyuk H, Calabrese F, Kümmel S, Musat F, Richnow HH, Musat N. Calculation of single cell assimilation rates from SIP-nanoSIMS-derived isotope ratios: a comprehensive approach. Front Microbiol. 2018;9:2342.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Arandia‐Gorostidi N, Alonso‐Sáez L, Stryhanyuk H, Richnow HH, Morán XAG, Musat N. Warming the phycosphere: Differential effect of temperature on the use of diatom‐derived carbon by two copiotrophic bacterial taxa. Environ Microbiol. 2020;22:1381–96.PubMed 
    Article 

    Google Scholar 
    Mayali X, Weber PK, Pett-Ridge J. Taxon-specific C/N relative use efficiency for amino acids in an estuarine community. FEMS Microbiol Ecol. 2013;83:402–12.CAS 
    PubMed 
    Article 

    Google Scholar 
    Meyer NR, Fortney JL, Dekas AE. NanoSIMS sample preparation decreases isotope enrichment: magnitude, variability and implications for single-cell rates of microbial activity. Environ Microbiol. 2021;23:81–98.CAS 
    PubMed 
    Article 

    Google Scholar 
    Kemp PF, Lee S, Laroche J. Estimating the growth rate of slowly growing marine bacteria from RNA content. Appl Environ Microbiol. 1993;59:2594–601.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Baltar F, Arístegui J, Gasol J, Sintes E, van Aken H, Herndl G. High dissolved extracellular enzymatic activity in the deep central Atlantic Ocean. Aquat Micro Ecol. 2010;58:287–302.Article 

    Google Scholar 
    Lønborg C, Nieto-Cid M, Hernando-Morales V, Hernández-Ruiz M, Teira E, Álvarez-Salgado XA. Photochemical alteration of dissolved organic matter and the subsequent effects on bacterial carbon cycling and diversity. FEMS Microbiol Ecol. 2016;92:fiw048.PubMed 
    Article 

    Google Scholar 
    Nagata T, Fukuda H, Fukuda R, Koike I. Bacter-ioplankton distribution and production in deep Pacific waters: large-scale geographic variations and possible coupling with sinking particle fluxes. Limnol Oceanogr. 2000;45:426–35.CAS 
    Article 

    Google Scholar 
    Teira E, Reinthaler T, Pernthaler A, Pernthaler J, Herndl GJ. Combining catalyzed reporter deposition-fluorescence in situ hybridization and microautoradiography to detect substrate utilization by bacteria and Archaea in the deep ocean. Appl Environ Microbiol. 2004;70:4411–4.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Mestre M, Hofer J. The microbial conveyor belt: connecting the globe through dispersion and dormancy. Trends Microbiol. 2020;29:482–92.PubMed 
    Article 

    Google Scholar 
    Giering SLC, Evans C. Overestimation of prokaryotic production by leucine incorporation—and how to avoid it. Limnol Oceanogr. 2022;67:726–38.Article 

    Google Scholar 
    Amos CM, Castelao RM, Medeiros PM. Offshore transport of particulate organic carbon in the California Current System by mesoscale eddies. Nat Commun. 2019;10:4940.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bauer JE, Druffel ERM. Ocean margins as a significant source of organic matter to the deep open ocean. Nature. 1998;392:482–5.CAS 
    Article 

    Google Scholar 
    Tamburini C, Boutrif M, Garel M, Colwell RR, Deming JW. Prokaryotic responses to hydrostatic pressure in the ocean—a review. Environ Microbiol. 2013;15:1262–74.CAS 
    PubMed 
    Article 

    Google Scholar 
    Arrieta JM, Mayol E, Hansman RL, Herndl GJ, Dittmar T, Duarte CM. Dilution limits dissolved organic carbon utilization in the deep ocean. Science. 2015;348:331–3.CAS 
    PubMed 
    Article 

    Google Scholar 
    Alonso C, Musat N, Adam B, Kuypers M, Amann R. HISH-SIMS analysis of bacterial uptake of algal-derived carbon in the Río de la Plata estuary. Syst Appl Microbiol. 2012;35:541–8.CAS 
    PubMed 
    Article 

    Google Scholar 
    Klawonn I, Bonaglia S, Whitehouse MJ, Littmann S, Tienken D, Kuypers MMM, et al. Untangling hidden nutrient dynamics: rapid ammonium cycling and single-cell ammonium assimilation in marine plankton communities. ISME J. 2019;13:1960–74.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Campbell BJ, Yu L, Heidelberg JF, Kirchman DL. Activity of abundant and rare bacteria in a coastal ocean. Proc Natl Acad Sci USA. 2011;108:12776–81.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kirchman DL. Growth rates of microbes in the oceans. Annu Rev Mar Sci. 2016;8:150720190448005.Article 

    Google Scholar 
    Blazewicz SJ, Barnard RL, Daly RA, Firestone MK. Evaluating rRNA as an indicator of microbial activity in environmental communities: limitations and uses. ISME J. 2013;7:2061–8.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Licht TR, Tolker-Nielsen T, Holmstrøm K, Krogfelt KA, Molin S. Inhibition of Escherichia coli precursor-16S rRNA processing by mouse intestinal contents. Environ Microbiol. 1999;1:23–32.CAS 
    PubMed 
    Article 

    Google Scholar 
    Sukenik A, Kaplan-Levy RN, Welch JM, Post AF. Massive multiplication of genome and ribosomes in dormant cells (akinetes) of Aphanizomenon ovalisporum (Cyanobacteria). ISME J. 2012;6:670–9.CAS 
    PubMed 
    Article 

    Google Scholar 
    Dekas AE, Connon SA, Chadwick GL, Trembath-Reichert E, Orphan VJ. Activity and interactions of methane seep microorganisms assessed by parallel transcription and FISH-NanoSIMS analyses. ISME J. 2016;10:678–92.CAS 
    PubMed 
    Article 

    Google Scholar 
    Wu J, Gao W, Johnson R, Zhang W, Meldrum D. Integrated metagenomic and metatranscriptomic analyses of microbial communities in the meso- and bathypelagic realm of North Pacific Ocean. Mar Drugs. 2013;11:3777–801.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ackermann M. A functional perspective on phenotypic heterogeneity in microorganisms. Nat Rev Microbiol. 2015;13:497–508.CAS 
    PubMed 
    Article 

    Google Scholar  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

    Silvopastoral systems and remnant forests enhance carbon storage in livestock-dominated landscapes in Mexico

    Song, X.-P. et al. Global land change from 1982 to 2016. Nature 560, 639–643 (2018).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Houghton, R. A. & Nassikas, A. A. Global and regional fluxes of carbon from land use and land cover change 1850–2015. Glob. Biogeochem. Cycles 31, 456–472 (2017).ADS 
    CAS 
    Article 

    Google Scholar 
    Phelps, L. N. & Kaplan, J. O. Land use for animal production in global change studies: Defining and characterizing a framework. Glob. Change Biol. 23, 4457–4471 (2017).ADS 
    Article 

    Google Scholar 
    Curtis, P. G., Slay, C. M., Harris, N. L., Tyukavina, A. & Hansen, M. C. Classifying drivers of global forest loss. Science 361, 1108–1111 (2018).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Hong, C. et al. Global and regional drivers of land-use emissions in 1961–2017. Nature 589, 554–561 (2021).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Knorr, W., Prentice, I. C., House, J. & Holland, E. Long-term sensitivity of soil carbon turnover to warming. Nature 433, 298–301 (2005).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Shi, Z. et al. The age distribution of global soil carbon inferred from radiocarbon measurements. Nat. Geosci. 13, 555–559 (2020).ADS 
    CAS 
    Article 

    Google Scholar 
    Sanderman, J., Hengl, T. & Fiske, G. J. Soil carbon debt of 12,000 years of human land use. Proc. Natl. Acad. Sci. 114, 9575–9580 (2017).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lal, R. Soil carbon sequestration impacts on global climate change and food security. Science 304, 1623–1627 (2004).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Friedlingstein, P. et al. Global carbon budget 2020. Earth Syst. Sci. Data 12, 3269–3340 (2020).ADS 
    Article 

    Google Scholar 
    Yue, C., Ciais, P., Houghton, R. A. & Nassikas, A. A. Contribution of land use to the interannual variability of the land carbon cycle. Nat. Commun. 11, 1–11 (2020).Article 

    Google Scholar 
    Zomer, R. J. et al. Global tree cover and biomass carbon on agricultural land: The contribution of agroforestry to global and national carbon budgets. Sci. Rep. 6, 1–12 (2016).Article 

    Google Scholar 
    De Stefano, A. & Jacobson, M. G. Soil carbon sequestration in agroforestry systems: a meta-analysis. Agrofor. Syst. 92, 285–299 (2018).
    Google Scholar 
    Bossio, D. et al. The role of soil carbon in natural climate solutions. Nat. Sustain. 3, 391–398 (2020).Article 

    Google Scholar 
    England, J. R., O’Grady, A. P., Fleming, A., Marais, Z. & Mendham, D. Trees on farms to support natural capital: An evidence-based review for grazed dairy systems. Sci. Total Environ. 704, 135345 (2020).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Ma, Z., Chen, H. Y., Bork, E. W., Carlyle, C. N. & Chang, S. X. Carbon accumulation in agroforestry systems is affected by tree species diversity, age and regional climate: A global meta-analysis. Glob. Ecol. Biogeogr. 29, 1817–1828 (2020).Article 

    Google Scholar 
    FAOSTAT. Data/Inputs/land use. In: Food Agriculture Organization. http://www.fao.org/faostat/en/#data/RL. (2020). Accessed 12 Sept 2020.Shukla, P. R. et al. Climate Change and Land: an IPCC special report on climate change, desertification, land degradation, sustainable land management, food security, and greenhouse gas fluxes in terrestrial ecosystems. (Intergovernmental Panel on Climate Change, 2019).Galdino, S. et al. Large-scale modeling of soil erosion with RUSLE for conservationist planning of degraded cultivated Brazilian pastures. Land Degrad. Dev. 27, 773–784 (2016).Article 

    Google Scholar 
    Stanimirova, R. et al. Sensitivity of global pasturelands to climate variation. Earth’s Future 7, 1353–1366 (2019).ADS 
    Article 

    Google Scholar 
    Tolimir, M. et al. The conversion of forestland into agricultural land without appropriate measures to conserve SOM leads to the degradation of physical and rheological soil properties. Sci. Rep. 10, 1–12 (2020).Article 

    Google Scholar 
    Mendoza-Ponce, A., Corona-Núñez, R., Kraxner, F., Leduc, S. & Patrizio, P. Identifying effects of land use cover changes and climate change on terrestrial ecosystems and carbon stocks in Mexico. Glob. Environ. Change. 53, 12–23 (2018).Article 

    Google Scholar 
    Castillo-Santiago, M., Hellier, A., Tipper, R. & De Jong, B. Carbon emissions from land-use change: An analysis of causal factors in Chiapas, Mexico. Mitig. Adapt. Strat. Glob. Change 12, 1213–1235 (2007).Article 

    Google Scholar 
    Kolb, M. & Galicia, L. Scenarios and story lines: drivers of land use change in southern Mexico. Environ. Dev. Sustain. 20, 681–702 (2018).Article 

    Google Scholar 
    Aryal, D. R. et al. Biomass accumulation in forests with high pressure of fuelwood extraction in Chiapas, Mexico. Revista Árvore 42, e420307 (2018).Article 

    Google Scholar 
    Aryal, D. R. et al. Soil organic carbon depletion from forests to grasslands conversion in Mexico: A review. Agriculture 8, 181 (2018).CAS 
    Article 

    Google Scholar 
    Griscom, B. W. et al. Natural climate solutions. Proc. Natl. Acad. Sci. 114, 11645–11650 (2017).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Chapman, M. et al. Large climate mitigation potential from adding trees to agricultural lands. Glob. Change Biol. 26, 4357–4365 (2020).ADS 
    Article 

    Google Scholar 
    Hayek, M. N., Harwatt, H., Ripple, W. J. & Mueller, N. D. The carbon opportunity cost of animal-sourced food production on land. Nat. Sustain. 4, 21–24 (2021).Article 

    Google Scholar 
    Kothandaraman, S., Dar, J. A., Sundarapandian, S., Dayanandan, S. & Khan, M. L. Ecosystem-level carbon storage and its links to diversity, structural and environmental drivers in tropical forests of Western Ghats, India. Sci. Rep. 10, 1–15 (2020).Article 

    Google Scholar 
    Havlík, P. et al. Climate change mitigation through livestock system transitions. Proc. Natl. Acad. Sci. 111, 3709–3714 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Resende, L. O. et al. Silvopastoral management of beef cattle production for neutralizing the environmental impact of enteric methane emission. Agroforestry Syst. 94, 893–903 (2020).Article 

    Google Scholar 
    Sans, G. H. C., Verón, S. R. & Paruelo, J. M. Forest strips increase connectivity and modify forests’ functioning in a deforestation hotspot. J. Environ. Manage. 290, 112606 (2021).Article 

    Google Scholar 
    Searchinger, T. D., Wirsenius, S., Beringer, T. & Dumas, P. Assessing the efficiency of changes in land use for mitigating climate change. Nature 564, 249–253 (2018).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Lawson, G., Dupraz, C. & Watté, J. Can silvoarable systems maintain yield, resilience, and diversity in the face of changing environments? in Agroecosystem Diversity 145–168 (Elsevier, 2019).Ramakrishnan, S. et al. Silvopastoral system for resilience of key soil health indicators in semi-arid environment. Arch. Agron. Soil Sci. 67, 1834–1847 (2021).CAS 
    Article 

    Google Scholar 
    Gerber, P. J. et al. Tackling Climate Change Through Livestock: A Global Assessment of Emissions and Mitigation Opportunities (Food and Agriculture Organization of the United Nations (FAO), 2013).
    Google Scholar 
    Haberl, H. Method précis: Human appropriation of net primary production (HANPP). In Social Ecology. Society-Nature Relations across Time and Space (eds Haberl, H. et al.) 332–334 (Springer Nature, 2016).
    Google Scholar 
    Smith, P. et al. Global change pressures on soils from land use and management. Glob. Change Biol. 22, 1008–1028 (2016).ADS 
    Article 

    Google Scholar 
    Herrero, M. et al. Greenhouse gas mitigation potentials in the livestock sector. Nat. Clim. Change. 6, 452–461 (2016).ADS 
    Article 

    Google Scholar 
    Lorenz, K. & Lal, R. Soil organic carbon sequestration in agroforestry systems. A review. Agron. Sustain. Develop. 34, 443–454 (2014).CAS 
    Article 

    Google Scholar 
    Michalk, D. L. et al. Sustainability and future food security—A global perspective for livestock production. Land Degrad. Dev. 30, 561–573 (2019).Article 

    Google Scholar 
    Bardgett, R. D. et al. Combatting global grassland degradation. Nat. Rev. Earth Environ. 2, 720–735 (2021).ADS 
    Article 

    Google Scholar 
    Pinheiro, F. M., Nair, P. R., Nair, V. D., Tonucci, R. G. & Venturin, R. P. Soil carbon stock and stability under Eucalyptus-based silvopasture and other land-use systems in the Cerrado biodiversity hotspot. J. Environ. Manage. 299, 113676 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Jose, S., Walter, D. & Kumar, B. M. Ecological considerations in sustainable silvopasture design and management. Agrofor. Syst. 93, 317–331 (2019).Article 

    Google Scholar 
    Oldfield, E. E. et al. Crediting agricultural soil carbon sequestration. Science 375, 1222–1225 (2022).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Udawatta, R. P., Walter, D. & Jose, S. Carbon sequestration by forests and agroforests: A reality check for the United States. Carbon Footprints 1, 8 (2022).Article 

    Google Scholar 
    Adame-Castro, D. E. et al. Diurnal and seasonal variations on soil CO2 fluxes in tropical silvopastoral systems. Soil Use Manag. 36, 671–681 (2020).Article 

    Google Scholar 
    Contosta, A. R., Asbjornsen, H., Orefice, J., Perry, A. & Smith, R. G. Climate consequences of temperate forest conversion to open pasture or silvopasture. Agric. Ecosyst. Environ. 333, 107972 (2022).CAS 
    Article 

    Google Scholar 
    Vargas-Zeppetello, L. R. et al. Consistent cooling benefits of silvopasture in the tropics. Nat. Commun. 13, 1–9 (2022).
    Google Scholar 
    Casanova-Lugo, F. et al. Effect of tree shade on the yield of Brachiaria brizantha grass in tropical livestock production systems in Mexico. Rangel. Ecol. Manage. 80, 31–38 (2022).Article 

    Google Scholar 
    Valenzuela Que, F. G. et al. Silvopastoral systems improve carbon stocks at livestock ranches in Tabasco, Mexico. Soil Use Manag. 38, 1237–1249 (2022).Article 

    Google Scholar 
    Nair, P. R. Classification of agroforestry systems. Agrofor. Syst. 3, 97–128 (1985).Article 

    Google Scholar 
    Somarriba, E., Kass, D. & Ibrahim, M. Definition and classification of agroforestry systems. Agroforestry Prototypes for Belize. Agroforestry Project. CATIE (Tropical Agricultural Research and Higher Education Center), Costa rica 3 (1998).Schroth, G. et al. Agroforestry and Biodiversity Conservation in Tropical Landscapes (Island Press, 2004).
    Google Scholar 
    Harvey, C. A. et al. Patterns of animal diversity in different forms of tree cover in agricultural landscapes. Ecol. Appl. 16, 1986–1999 (2006).PubMed 
    Article 

    Google Scholar 
    Cardinael, R., Mao, Z., Chenu, C. & Hinsinger, P. Belowground functioning of agroforestry systems: Recent advances and perspectives. Plant Soil. 1–13 (2020).Ibrahim, M. & Beer, J. Agroforestry Prototypes for Belize Vol. 28 (CATIE, 1998).
    Google Scholar 
    Ibrahim, M., Villanueva, C., Casasola, F. & Rojas, J. Sistemas silvopastoriles como una herramienta para el mejoramiento de la productividad y restauración de la integridad ecológica de paisajes ganaderos. Pastos y Forrajes 29, 383–419 (2006).
    Google Scholar 
    Phalan, B., Onial, M., Balmford, A. & Green, R. E. Reconciling food production and biodiversity conservation: Land sharing and land sparing compared. Science 333, 1289–1291 (2011).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Van Zanten, H. H. et al. Defining a land boundary for sustainable livestock consumption. Glob. Change Biol. 24, 4185–4194 (2018).ADS 
    Article 

    Google Scholar 
    Torres, C. M. M. E. et al. Greenhouse gas emissions and carbon sequestration by agroforestry systems in southeastern Brazil. Sci. Rep. 7, 1–7 (2017).Article 

    Google Scholar 
    Haile, S. G., Nair, V. D. & Nair, P. R. Contribution of trees to carbon storage in soils of silvopastoral systems in Florida, USA. Glob. Change Biol. 16, 427–438 (2010).ADS 
    Article 

    Google Scholar 
    Chatterjee, N., Nair, P. R., Chakraborty, S. & Nair, V. D. Changes in soil carbon stocks across the Forest-Agroforest-Agriculture/Pasture continuum in various agroecological regions: A meta-analysis. Agric. Ecosyst. Environ. 266, 55–67 (2018).Article 

    Google Scholar 
    Aynekulu, E. et al. Carbon storage potential of silvopastoral systems of Colombia. Land 9, 309 (2020).Article 

    Google Scholar 
    Birkhofer, K. et al. Land-use type and intensity differentially filter traits in above-and below-ground arthropod communities. J. Anim. Ecol. 86, 511–520 (2017).PubMed 
    Article 

    Google Scholar 
    Dahlsjö, C. A. et al. The local impact of macrofauna and land-use intensity on soil nutrient concentration and exchangeability in lowland tropical Peru. Biotropica 52, 242–251 (2020).Article 

    Google Scholar 
    Vizcaíno-Bravo, Q., Williams-Linera, G. & Asbjornsen, H. Biodiversity and carbon storage are correlated along a land use intensity gradient in a tropical montane forest watershed, Mexico. Basic Appl. Ecol. 44, 24–34 (2020).Article 

    Google Scholar 
    Villanueva-López, G., Martínez-Zurimendi, P., Ramírez-Avilés, L., Aryal, D. R. & Casanova-Lugo, F. Live fences reduce the diurnal and seasonal fluctuations of soil CO 2 emissions in livestock systems. Agron. Sustain. Dev. 36, 23 (2016).Article 

    Google Scholar 
    López-Santiago, J. G. et al. Carbon storage in a silvopastoral system compared to that in a deciduous dry forest in Michoacán, Mexico. Agroforestry Syst. 93, 199–211 (2019).Article 

    Google Scholar 
    Aryal, D. R., Gómez-González, R. R., Hernández-Nuriasmú, R. & Morales-Ruiz, D. E. Carbon stocks and tree diversity in scattered tree silvopastoral systems in Chiapas, Mexico. Agroforestry Syst. 93, 213–227 (2019).Article 

    Google Scholar 
    Beckert, M. R., Smith, P., Lilly, A. & Chapman, S. J. Soil and tree biomass carbon sequestration potential of silvopastoral and woodland-pasture systems in North East Scotland. Agrofor. Syst. 90, 371–383 (2016).Article 

    Google Scholar 
    Cárdenas, A., Moliner, A., Hontoria, C. & Ibrahim, M. Ecological structure and carbon storage in traditional silvopastoral systems in Nicaragua. Agrofor. Syst. 93, 229–239 (2019).Article 

    Google Scholar 
    Lehmann, J. et al. Persistence of soil organic carbon caused by functional complexity. Nat. Geosci. 13, 529–534 (2020).ADS 
    CAS 
    Article 

    Google Scholar 
    Amézquita, M. C., Ibrahim, M., Llanderal, T., Buurman, P. & Amézquita, E. Carbon sequestration in pastures, silvo-pastoral systems and forests in four regions of the Latin American tropics. J. Sustain. For. 21, 31–49 (2004).Article 

    Google Scholar 
    Rosenstock, T. S. et al. Making trees count: Measurement and reporting of agroforestry in UNFCCC national communications of non-Annex I countries. Agric. Ecosyst. Environ. 284, 106569 (2019).Article 

    Google Scholar 
    Junior, M. A. L., Fracetto, F. J. C., da Silva Ferreira, J., Silva, M. B. & Fracetto, G. G. M. Legume-based silvopastoral systems drive C and N soil stocks in a subhumid tropical environment. CATENA 189, 104508 (2020).Article 

    Google Scholar 
    Villanueva-Partida, C. et al. Influence of the density of scattered trees in pastures on the structure and species composition of tree and grass cover in southern Tabasco, Mexico. Agric. Ecosyst. Environ. 232, 1–8 (2016).Article 

    Google Scholar 
    Morantes-Toloza, J. L. & Renjifo, L. M. Live fences in tropical production systems: A global review of uses and perceptions. Rev. Biol. Trop. 66, 739–753 (2018).Article 

    Google Scholar 
    MoralesRuiz, D. E. et al. Carbon contents and fine root production in tropical silvopastoral systems. Land Degrad. Develop. 32, 738–756 (2021).Article 

    Google Scholar 
    Hoosbeek, M. R., Remme, R. P. & Rusch, G. M. Trees enhance soil carbon sequestration and nutrient cycling in a silvopastoral system in south-western Nicaragua. Agrofor. Syst. 92, 263–273 (2018).
    Google Scholar 
    Aryal, D. R. et al. Fine wood decomposition rates decline with the sge of tropical successional forests in Southern Mexico: Implications to ecosystem carbon storage. Ecosystems 25, 661–677 (2022).CAS 
    Article 

    Google Scholar 
    Dignac, M.-F. et al. Increasing soil carbon storage: Mechanisms, effects of agricultural practices and proxies. A review. Agron. Sustain. Develop. 37, 1–27 (2017).CAS 
    Article 

    Google Scholar 
    Sánchez-Silva, S. et al. Fine root biomass stocks but not the production and turnover rates vary with the age of tropical successional forests in Southern Mexico. Rhizosphere 21, 100474 (2022).Article 

    Google Scholar 
    Montejo-Martínez, D. et al. Fine root density and vertical distribution of Leucaena leucocephala and grasses in silvopastoral systems under two harvest intervals. Agrofor. Syst. 94, 843–855 (2020).Article 

    Google Scholar 
    Sánchez-Silva, S., De Jong, B. H., Aryal, D. R., Huerta-Lwanga, E. & Mendoza-Vega, J. Trends in leaf traits, litter dynamics and associated nutrient cycling along a secondary successional chronosequence of semi-evergreen tropical forest in South-Eastern Mexico. J. Trop. Ecol. 34, 364–377 (2018).Article 

    Google Scholar 
    Waters, C. M., Orgill, S. E., Melville, G. J., Toole, I. D. & Smith, W. J. Management of grazing intensity in the semi-arid rangelands of Southern Australia: Effects on soil and biodiversity. Land Degrad. Dev. 28, 1363–1375 (2017).Article 

    Google Scholar 
    Baldassini, P. & Paruelo, J. M. Deforestation and current management practices reduce soil organic carbon in the semi-arid Chaco, Argentina. Agric. Syst. 178, 102749 (2020).Article 

    Google Scholar 
    Abdalla, M. et al. Critical review of the impacts of grazing intensity on soil organic carbon storage and other soil quality indicators in extensively managed grasslands. Agric. Ecosyst. Environ. 253, 62–81 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lange, M. et al. Plant diversity increases soil microbial activity and soil carbon storage. Nat. Commun. 6, 1–8 (2015).ADS 
    Article 

    Google Scholar 
    Wiesmeier, M. et al. Soil organic carbon storage as a key function of soils—A review of drivers and indicators at various scales. Geoderma 333, 149–162 (2019).ADS 
    CAS 
    Article 

    Google Scholar 
    Lim, S.-S. et al. Soil organic carbon stocks in three Canadian agroforestry systems: From surface organic to deeper mineral soils. For. Ecol. Manage. 417, 103–109 (2018).ADS 
    Article 

    Google Scholar 
    Nair, P. Carbon sequestration studies in agroforestry systems: A reality-check. Agrofor. Syst. 86, 243–253 (2012).Article 

    Google Scholar 
    Montagnini, F., Ibrahim, M. & Murgueitio, E. Silvopastoral systems and climate change mitigation in Latin America. Bois et forêts des tropiques 316, 3–16 (2013).Article 

    Google Scholar 
    Allison, S. D., Wallenstein, M. D. & Bradford, M. A. Soil-carbon response to warming dependent on microbial physiology. Nat. Geosci. 3, 336–340 (2010).ADS 
    CAS 
    Article 

    Google Scholar 
    Sarto, M. V. et al. Soil microbial community and activity in a tropical integrated crop-livestock system. Appl. Soil. Ecol. 145, 103350 (2020).Article 

    Google Scholar 
    Malik, A. A. et al. Land use driven change in soil pH affects microbial carbon cycling processes. Nat. Commun. 9, 1–10 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    Bautista, F., Palacio-Aponte, G., Quintana, P. & Zinck, J. A. Spatial distribution and development of soils in tropical karst areas from the Peninsula of Yucatan, Mexico. Geomorphology 135, 308–321 (2011).ADS 
    Article 

    Google Scholar 
    Kaiser, M. et al. The influence of mineral characteristics on organic matter content, composition, and stability of topsoils under long‐term arable and forest land use. J. Geophys. Res. Biogeosci. 117, (2012).Castillo, M. S., Tiezzi, F. & Franzluebbers, A. J. Tree species effects on understory forage productivity and microclimate in a silvopasture of the Southeastern USA. Agric. Ecosyst. Environ. 295, 106917 (2020).Article 

    Google Scholar 
    Yang, Y., Tilman, D., Furey, G. & Lehman, C. Soil carbon sequestration accelerated by restoration of grassland biodiversity. Nat. Commun. 10, 1–7 (2019).
    Google Scholar 
    Grass, I. et al. Land-sharing/-sparing connectivity landscapes for ecosystem services and biodiversity conservation. People Nat. 1, 262–272 (2019).
    Google Scholar 
    Orefice, J., Smith, R. G., Carroll, J., Asbjornsen, H. & Howard, T. Forage productivity and profitability in newly-established open pasture, silvopasture, and thinned forest production systems. Agrofor. Syst. 93, 51–65 (2019).Article 

    Google Scholar 
    Aryal, D. R. et al. Potencial de almacenamiento de carbono en áreas forestales en un sistema ganadero. Revista mexicana de ciencias forestales 9, 150–180 (2018).Article 

    Google Scholar 
    Gobierno de la Republica. Intended Nationally Determined Contribution, Mexico. (Instituto Nacional de Ecología y Cambio Climático, Mexico City, 2015).Bonilla-Moheno, M. & Aide, T. M. Beyond deforestation: Land cover transitions in Mexico. Agric. Syst. 178, 102734 (2020).Article 

    Google Scholar 
    INEGI. Mapa de uso de suelo y vegetación de México: Series I–VII. Instituto Nacional de Estadística y Geografía (INEGI), Aguascalientes, Mexico. https://www.inegi.org.mx/temas/usosuelo/#Map (2018). Accessed 17 Aug 2022.Gosling, E., Reith, E., Knoke, T. & Paul, C. A goal programming approach to evaluate agroforestry systems in Eastern Panama. J. Environ. Manage. 261, 110248 (2020).PubMed 
    Article 

    Google Scholar 
    Bergier, I. et al. Could bovine livestock intensification in Pantanal be neutral regarding enteric methane emissions?. Sci. Total Environ. 655, 463–472 (2019).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Barkin, D. E. uso de la tierra agrícola en Mexico. Problemas del Desarrollo 12, 59–85 (1981).
    Google Scholar 
    Valdivieso-Pérez, I. A., García-Barrios, L. E., Álvarez-Solís, D. & Nahed-Toral, J. From cornfields to grasslands: Change in the quality of soil. Terra Latinoamericana. 30, 363–374 (2012).
    Google Scholar 
    Goldstein, A. et al. Protecting irrecoverable carbon in Earth’s ecosystems. Nat. Clim. Chang. 10, 287–295 (2020).ADS 
    CAS 
    Article 

    Google Scholar 
    CONAFOR. Acciones Tempranas REDD+ Mexico. https://www.gob.mx/conafor/documentos/acciones-tempranas-redd (2017). Accessed 04 Oct 2020.CATIE. Bidiversidad y paisajes ganaderos agrosilvopastoriles sostenibles. https://www.biopasos.com (2020). Accessed 04 Oct 2020.Freire-Santos, P. Z. F., Crouzeilles, R. & Sansevero, J. B. B. Can agroforestry systems enhance biodiversity and ecosystem service provision in agricultural landscapes? A meta-analysis for the Brazilian Atlantic Forest. For. Ecol. Manage. 433, 140–145 (2019).Article 

    Google Scholar 
    Zanne, A. et al. Data from: Towards a worldwide wood economics spectrum. (2009). 10.5061/dryad.234.Chave, J. et al. Improved allometric models to estimate the aboveground biomass of tropical trees. Glob. Change Biol. 20, 3177–3190 (2014).ADS 
    Article 

    Google Scholar 
    Bojórquez, A. et al. Improving the accuracy of aboveground biomass estimations in secondary tropical dry forests. For. Ecol. Manage. 474, 118384 (2020).Article 

    Google Scholar 
    Cairns, M. A., Brown, S., Helmer, E. H. & Baumgardner, G. A. Root biomass allocation in the world’s upland forests. Oecologia 111, 1–11 (1997).ADS 
    PubMed 
    Article 

    Google Scholar 
    Shannon, C.E., Weaver. A Mathematical Theory of Communication Vol. 27 (University of Illinois Press, 1964).Sorensen, T. A. A method of establishing groups of equal amplitude in plant sociology based on similarity of species content and its application to analyses of the vegetation on Danish commons. Biol. Skar. 5, 1–34 (1948).
    Google Scholar 
    Pielou, E. C. The measurement of diversity in different types of biological collections. J. Theor. Biol. 13, 131–144 (1966).ADS 
    Article 

    Google Scholar 
    Van Wagner, C. Practical Aspects of the Line Intersect Method Vol. 12 (Canadian Forestry Service, 1982).
    Google Scholar 
    Heanes, D. Determination of total organic-C in soils by an improved chromic acid digestion and spectrophotometric procedure. Commun. Soil Sci. Plant Anal. 15, 1191–1213 (1984).CAS 
    Article 

    Google Scholar  More

  • in

    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